Abstract
Sharks are essential components of marine communities, and their removal might simplify ecosystems and lead to unpredictable and detrimental effects on the food web. Comparing the isotopic niche of species between archaeological and modern communities can provide information to assess temporal changes in the ecological dynamics of communities. Here, stable isotope analysis was used to compare food web topology metrics between two shark guilds or communities, a late Holocene archaeological community (AC) dating from 700 to 500 years ago and a modern community (MC) trophic web, both from South Brazil. In the same line of comparison, we assess the trophic position of a top predator, Carcharias taurus. Results showed topological temporal differences such as higher trophic redundancy and higher patterns of niche overlap in the AC. Higher trophic redundancy could be expected in late Holocene food webs, as similar studies also observed these findings. In contrast, the MC showed less dense packing of species within the isotopic niche space, thus higher niche partitioning and higher trophic diversity, suggesting changing ecological interaction dynamics. We found that Carcharias taurus has increased its trophic level, possibly due to a release from the intraspecific competition and a dietary shift towards larger prey items. We suggest that anthropic impacts, such as overfishing, may cause these differences in the trophic position of this species. We also advocate that this study method might help future trophic reconstructions using shark teeth, as information about past marine environments is scarce, and could serve as a baseline for future studies.
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References
Barreto RR, Ferretti F, Flemming JM, Amorim A, Andrade H, Worm B, Lessa R (2016) Trends in the exploitation of South Atlantic shark populations. Conserv Biol 30:792–804. https://doi.org/10.1111/cobi.12663
Bas M, Briz I Godino I, 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. Glob Chang Biol 2:404–419. https://doi.org/10.1111/gcb.14523
Bascompte J, Melián CJ, Sala E (2005) Interaction strength combinations and the overfishing of a marine food web. Proc Natl Acad Sci U S A 102:5443–5447. https://doi.org/10.1073/pnas.0501562102
Baum JK, Worm B (2009) Cascading top-down effects of changing oceanic predator abundances. J Anim Ecol 78:699–714. https://doi.org/10.1111/j.1365-2656.2009.01531.x
Belle S, Cabana G (2020) Effects of changes in isotopic baselines on the evaluation of food web structure using isotopic functional indices. PeerJ. https://doi.org/10.7717/peerj.9999
Bolnick DI, Ingram T, Stutz WE, Snowber LK, Lau OL, Paull JS (2010) Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proc R Soc B Biol Sci 277:1789–1797. https://doi.org/10.1098/rspb.2010.0018
Bornatowski H, Braga RR, Abilhoa V, Corrêa MFM (2014a) Feeding ecology and trophic comparisons of six shark species in a coastal ecosystem off southern Brazil. J Fish Biol 85:246–263. https://doi.org/10.1111/jfb.12417
Bornatowski H, Navia AF, Braga RR, Abilhoa V, Corrêa MFM (2014b) Ecological importance of sharks and rays in a structural foodweb analysis in southern Brazil. ICES J Mar Sci 71:1586–1592. https://doi.org/10.1093/icesjms/fsu025
Bornatowski H, Angelini R, Coll M, Barreto RRP, Amorim AF (2018) Ecological role and historical trends of large pelagic predators in a subtropical marine ecosystem of the South Atlantic. Rev Fish Biol Fish 28:241–259. https://doi.org/10.1007/s11160-017-9492-z
Burg Mayer G, de Souza ECS, Gilson S-P, Freitas RHA (2022) South Brazil pre-colonial sharks: insights into biodiversity and species distributions. J Fish Biol 100(3):811–819. https://doi.org/10.1111/jfb.14998
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
Chiessi CM, Mulitza S, Groeneveld J, Silva JB, Campos MC, Gurgel MHC (2014) Variability of the Brazil Current during the late Holocene. Palaeogeogr Palaeoclimatol Palaeoecol 415:28–36. https://doi.org/10.1016/j.palaeo.2013.12.005
Cortés (1999) Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci 56:707–717. https://doi.org/10.1006/jmsc.1999.0489
DeNiro MJ (1985) Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature 317:806–809. https://doi.org/10.1038/317806a0
Dobberstein RC, Collins MJ, Craig OE, Taylor G, Penkman KEH, Ritz-Timme S (2009) Archaeological collagen: Why worry about collagen diagenesis? Archaeol Anthropol Sci 1:31–42. https://doi.org/10.1007/s12520-009-0002-7
Doney SC, Ruckelshaus M, Duffy EJ, Barry JP, Chan F, English CA, Talley LD (2012) Climate change impacts on marine ecosystems. Ann Rev Mar Sci 4(1):11–37. https://doi.org/10.1146/annurev-marine-041911-111611
Drago M, Crespo E, Aguilar A, Cardona L, Garcia N, Dans SL, Goodall N (2009) Historic diet change of the South American sea lion in Patagonia as revealed by isotopic analysis. Mar Ecol Prog Ser 384:273–286. https://doi.org/10.3354/meps08017
Drago M, Cardona L, Franco-Trecu V, Crespo EA, Vales DG, 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
Dulvy NK, Forrest RE (2010) Life histories, population dynamics, and extinction risks in chondrichthyans. Taylor & Francis, pp 655–696. https://doi.org/10.1201/9781420080483-24
Dulvy NK, Pacoureau N, Rigby CL et al (2021) Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Curr Biol 31:4773-4787.e8. https://doi.org/10.1016/j.cub.2021.08.062
Durante L, Wing S, Ingram T, Sabadel A, Shima J (2022) Changes in trophic structure of an exploited fish community at the centennial scale are linked to fisheries and climate forces. Sci Rep 12:1–12. https://doi.org/10.1038/s41598-022-08391-x
Ebert DA, Fowler SL, Compagno LJ (2013) Sharks of the world: a fully illustrated guide. Wild Nature Press
Enax J, Prymak O, Raabe D, Epple M (2012) Structure, composition, and mechanical properties of shark teeth. J Struct Biol 178:290–299. https://doi.org/10.1016/j.jsb.2012.03.012
Erlandson JM, Rick TC (2008) Human impacts on ancient marine ecosystems, 1st edn. University of California Press, Los Angeles California USA
Estrada JA, Rice AN, Natanson LJ, Skomal GB (2006) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87:829–834. https://doi.org/10.1890/0012-9658(2006)87[829:uoiaov]2.0.co;2
Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecol Lett 13:1055–1071. https://doi.org/10.1111/j.1461-0248.2010.01489.x
Fossari TD (2004) A população pré-colonial Jê na paisagem da Ilha de Santa Catarina. PhD Thesis, Universidade Federal de Santa Catarina, Florianópolis, Brazil
Fossile T, Ferreira J, da Rocha Bandeira D et al (2019) Pre-Columbian fisheries catch reconstruction for a subtropical estuary in South America. Fish Fish 20(6):1124–1137. https://doi.org/10.1111/faf.12401
Gallagher AJ, Shiffman DS, Byrnes EE, Hammerschlag-Peyer CM, Hammerschlag N (2017) Patterns of resource use and isotopic niche overlap among three species of sharks occurring within a protected subtropical estuary. Aquat Ecol 51:435–448. https://doi.org/10.1007/s10452-017-9627-2
Gill AB (2003) The dynamics of prey choice in fish: the importance of prey size and satiation. J Fish Biol 63:105–116. https://doi.org/10.1111/j.1095-8649.2003.00214.x
Gilson SP, Lessa A (2019) Human-Sharks interaction in chroniclers’ accounts from the XVIth and XVIIth centuries: a rich source of information for Brazilian zooarchaeological studies. Archaeofauna 28:157–167. https://doi.org/10.15366/archaeofauna2019.28.013
Gilson S, Lessa A (2020) Ocupação tardia do litoral norte e central catarinense por grupos pescadores-caçadores-coletores: uma revisão críutica do contexto cronológico dos sítios rasos com presença de cerâmica. Rev De Arqueol 33:3–25. https://doi.org/10.24885/sab.v33i1.702
Gilson S-P, Lessa A (2021) Capture, processing and utilization of sharks in archaeological context: its importance among fisher-hunter-gatherers from southern Brazil. J Archaeol Sci Rep 35:102693. https://doi.org/10.1016/j.jasrep.2020.102693
Guiry EJ, Szpak P (2020) Quality control for modern bone collagen stable carbon and nitrogen isotope measurements. Methods Ecol Evol 11:1049–1060. https://doi.org/10.1111/2041-210X.13433
Heileman S, Gasalla M (2009) XVI-54 South Brazil Shelf: LME# 15. The UNEP ecosystem report: a perspective on changing conditions in LMEs of the World’s regional seas. UNEP Reg Seas Rep Stud 182:723–734
Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210. https://doi.org/10.1016/j.tree.2008.01.003
Hussey NE, MacNeil MA, Olin JA, McMeans BC, Kinney MJ, Chapman DD, Fisk AT (2012a) Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. J Fish Biol 80:1449–1484. https://doi.org/10.1111/j.1095-8649.2012.03251.x
Hussey NE, McCann HM, Cliff G, Dudley SF, Wintner SP, Fisk AT (2012b) Size-based analysis of diet and trophic position of the white shark, Carcharodon carcharias, in South African waters. Glob Perspect Biol Life Hist White Shark. https://doi.org/10.1201/b11532-5
Hussey NE, MacNeil MA, McMeans BC, Olin JA, Dudley SFJ, Cliff G, Wintner SP, Fennessy ST, Fisk AT (2014) Rescaling the trophic structure of marine food webs. Ecol Lett 17:239–250. https://doi.org/10.1111/ele.12226
Hussey NE, MacNeil MA, Siple MC, Popp BN, Dudley SFJ, Fisk AT (2015) Expanded trophic complexity among large sharks. Food Webs 4:1–7. https://doi.org/10.1016/j.fooweb.2015.04.002
Hutchinson EG (1957) Concluding remarks. population studies: animal ecology and demography. Cold Springs Harbor Symp Quant Biol 22:415–427
ICMBio Instituto Chico Mendes de Conservação da Biodiversidade (2018) Livro vermelho da fauna brasileira ameaçada de extinção. VI–Peixes
Indermühle A, Stocker TF, Joos F, Fischer H, Smith HJ, Wahler M, Deck B, Mastroianni D, Tschumi J, Blunier T, Meyer R, Stauffer B (1999) Holocene carbon-cycle dynamics based on CO2 trapped in ice at Taylor Dome, Antarctica. Nature 398:121–126. https://doi.org/10.1038/18158
Jabot F, Giraldo C, Lefebvre S, Dubois S (2017) Are food web structures well represented in isotopic spaces? Funct Ecol 31:1975–1984. https://doi.org/10.1111/1365-2435.12895
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, Lenihan 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
Jennings S (2005) Size-based analyses of aquatic food webs. Aquatic food webs: an ecosystem approach. Oxford University Press, Oxford, pp 86–97
Kemp NE (1984) Organic matrices and mineral crystallites in vertebrate scales, teeth and skeletons. Am Zool 24:965–976. https://doi.org/10.1093/icb/24.4.965
Kim SL, Koch PL (2012) Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environ Biol Fishes 95:53–63. https://doi.org/10.1007/s10641-011-9860-9
Kinney MJ, Hussey NE, Fisk AT, Tobin AJ, Simpfendorfer CA (2011) Communal or competitive? Stable isotope analysis provides evidence of resource partitioning within a communal shark nursery. Mar Ecol Prog Ser 439:263–276. https://doi.org/10.3354/meps09327
Kotas JE (2005) A pesca de emalhe e de espinhel-de-superfície na Região Sudeste-Sul do Brasil. Instituto Oceanográfico-USP
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
Layman CA, Araujo MS, Boucek R, Hammerschalg-Peyer CM, Harrison E, Jud ZR, Matich P, Rosenblatt AE, Vaudo JJ, Yeager LA, Post DM, Bearhop S (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev 87:545–562. https://doi.org/10.1111/j.1469-185x.2011.00208.x
LeGeros RZ (1981) Apatites in biological systems. Prog Cryst Growth Charact Mater 4:1–45. https://doi.org/10.1016/0146-3535(81)90046-0
Lopes MS, Bertucci TCP, Rapagnã L, Tubin RA, Monteiro-Neto C, Tomas ARG, Tenório MC, Lima T, Souza R, Carrillo-Briceño JD, Haimovici M, Macario K, Carvalho C, Aguilera Socorro O (2016) The path towards endangered species: prehistoric fisheries in southeastern Brazil. Plos one 11:e0154476. https://doi.org/10.1371/journal.pone.0154476
Lübke A, Enax J, Loza K, Prymak O, Gaengler P, Fabritius HO, Raabe D, Epple M (2015) Dental lessons from past to present: ultrastructure and composition of teeth from plesiosaurs, dinosaurs, extinct and recent sharks. RSC Adv 5:61612–61622. https://doi.org/10.1039/c5ra11560d
Lucifora LO, García VB, Escalante AH (2009) How can the feeding habits of the sand tiger shark influence the success of conservation programs? Anim Conserv 12:291–301. https://doi.org/10.1111/j.1469-1795.2009.00247.x
Lucifora LO, García VB, Worm B (2011) Global diversity hotspots and conservation priorities for sharks. PLoS One 6:e19356
Macarthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609. https://doi.org/10.1086/282454
Mahiques MM, Coaracy Wainer IK, Burone L, Nagai R, Mello e Souza SH, Figueira RCL, Silveira ICA, Bícego MC, Alves DPV, Hammer Ø (2009) A high-resolution Holocene record on the Southern Brazilian shelf: paleoenvironmental implications. Quat Int 206:52–61. https://doi.org/10.1016/j.quaint.2008.09.010
Mahiques MM, de Sousa SHM, Furtado VV, Tessler MG, Toledo FAL, Burone L, Figueira RCL, Klein DA, Martins CC, Alves DPV (2010) The southern Brazilian shelf: general characteristics, quaternary evolution and sediment distribution. Braz J Oceanogr 58:25–34. https://doi.org/10.1590/s1679-87592010000600004
Maureaud A, Gascuel D, Colléter M, Palomares MLD, Pontavice HD, Pauly D, Cheung WWL (2017) Global change in the trophic functioning of marine food webs. Plos one 12:e0182826. https://doi.org/10.1371/journal.pone.0182826
McClelland J, Valiela I (1998) Changes in food web structure under the influence of increased anthropogenic nitrogen inputs to estuaries. Mar Ecol Prog Ser 168:259–271. https://doi.org/10.3354/meps168259
Mendes AB, Duarte MR, Silva EP (2018) Biodiversity of Holocene marine fish of the southeast coast of Brazil. Biota Neotrop 18(1):e20170394. https://doi.org/10.1590/1676-0611-BN-2017-0394
Milessi AC, Arancibia H, Neira S, Defeo O (2005) The mean trophic level of Uruguayan landings during the period 1990–2001. Fish Res 74:223–231. https://doi.org/10.1016/j.fishres.2005.02.002
Montoya JM, Pimm SL, Solé RV (2006) Ecological networks and their fragility. Nature 442(7100):259–264
Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283. https://doi.org/10.1038/nature01610
Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850. https://doi.org/10.1126/science.1138657
Nagai RH, Sousa SHM, Mahiques MM (2014) Chapter 5 the southern Brazilian shelf. Geol Soc Lond Mem 41:47–54. https://doi.org/10.1144/m41.5
Pacoureau N, Rigby CL, Kyne PM, Sherley RB, Winker H, Carlson JK, Fordham SV, Barreto RP, Fernando D, Francis MP, Jabado RW, Herman KB, Liu K-M, Marshall AD, Pollom RA, Romanov EV, Simpfendorfer CA, Yin JS, Kindsvater HK, Dulvy NK (2021) Half a century of global decline in oceanic sharks and rays. Nat Rev. https://doi.org/10.1038/s41586-020-03173-9
Pauly D, Christensen V, Dalsgaard J et al (1998) Fishing down marine food webs. Science 279:860–863. https://doi.org/10.1126/science.279.5352.860
Pereira MD, Schettini CAF, Omachi CY (2009) Caracterização de feições oceanográficas na plataforma de Santa Catarina através de imagens orbitais. Revista Brasileira De Geofísica 27:81–93. https://doi.org/10.1590/s0102-261x2009000100007
Piola AR, Campos EJD, Möller OO et al (2000) Subtropical shelf front off eastern South America. J Geophys Res Oceans 105:6565–6578. https://doi.org/10.1029/1999jc000300
Quezada-Romegialli C, Jackson AL, Hayden B, Kahilainen KK, Lopes C, Harrod C (2018) tRophicPosition, an r package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods Ecol Evol 9:1592–1599. https://doi.org/10.1111/2041-210x.13009
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Reitz E, Wing E (2008) Zooarchaeology, 2ª. Cambridge University Press, Cambridge, England
Roff G, Doropoulos C, Rogers A, Bozec YM, Krueck NC, Aurellado E, Priest M, Birrell C, Mumby PJ (2016) The ecological role of sharks on coral reefs. Trends Ecol Evol 31:395–407. https://doi.org/10.1016/j.tree.2016.02.014
Santos MC, Faria-Junior E, Freitas RHA (2020) Reconhecimento etnoecológico sobre o tubarão-mangona Carcharias taurus sob a perspectiva de pescadores artesanais da grande Florianópolis-SC Brasil. Rev Nord Biol 27(1):143–157. https://doi.org/10.22478/ufpb.2236-1480.2019v27n1.47526
Saporiti F, Bearhop S, Silva L, Vales DG, Zenteno L, Crespo EA, Aguilar A, Cardona L (2014) Longer and less overlap** food webs in anthropically disturbed marine ecosystems: confirmations from the past. PloS One 9:e103132. https://doi.org/10.1371/journal.pone.0103132
Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88:2415–2426. https://doi.org/10.1890/06-0937.1
Shiffman DS, Gallagher AJ, Boyle MD, Hammerschlag-Peyer CM, Hammerschlag N (2012) Stable isotope analysis as a tool for elasmobranch conservation research: a primer for non-specialists. Mar Freshw Res 63:635. https://doi.org/10.1071/mf11235
Shiffman DS, Kaufman L, Heithaus M, Hammerschlag N (2019) Intraspecific differences in relative isotopic niche area and overlap of co-occurring sharks. Aquat Ecol. https://doi.org/10.1007/s10452-019-09685-5
Shimada K (2004) The relationship between the tooth size and total body length in the sandtiger shark, Carcharias taurus (Lamniformes: Odontaspididae). J Fossil Res 37:76–81
Shipley ON, Henkes GA, Gelsleichter J, Morgan CR, Schneider EV, Talwar BS, Frisk MG (2021) Shark tooth collagen stable isotopes (δ15N and δ13C) as ecological proxies. J Anim Ecol 90:2188–2201. https://doi.org/10.1111/1365-2656.13518
Smale MJ (2005) The diet of the ragged-tooth shark Carcharias taurus Rafinesque 1810 in the Eastern Cape, South Africa. Afr J Mar Sci 27:331–335. https://doi.org/10.2989/18142320509504091
Townsend CR, Winfield IJ (1985) The application of optimal foraging theory to feeding behavior. In: Tytler P, Calow P (eds) Fish energetics: new perspectives. John Hopkins University Press, Baltimore, pp 67–98. https://doi.org/10.1007/978-94-011-7918-8
Vales DG, Cardona L, Zangrando AF, Borella F, Saporiti F, Goodall RN, 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
Vandermeer JH (1972) Niche theory. Annu Rev Ecol Syst 3:107–132. https://doi.org/10.1146/annurev.es.03.110172.000543
Vander Zanden MJ, Rasmussen JB (1996) A trophic position model of pelagic food webs: impact on contaminant bioaccumulation in lake trout. Ecol Monogr 66:451–477. https://doi.org/10.2307/2963490
Vander-Zanden JM, Fetzer WW (2007) Global patterns of aquatic food chain length. Oikos 116:1378–1388. https://doi.org/10.1111/j.0030-1299.2007.16036.x
Vaudo J, Heithaus M (2011) Dietary niche overlap in a nearshore elasmobranch mesopredator community. Mar Ecol Prog Ser 425:247–260. https://doi.org/10.3354/meps08988
Vennemann T, Hegner E, Cliff G, Benz G (2001) Isotopic composition of recent shark teeth as a proxy for environmental conditions. Geochim Cosmochim Acta 65:1583–1599. https://doi.org/10.1016/s0016-7037(00)00629-3
Vooren CM, Klippel S (2005) Ações para a conservação de tubarões e raias no sul do Brasil. Igaré, Porto Alegre
White WT, Platell ME, Potter IC (2004) Comparisons between the diets of four abundant species of elasmobranchs in a subtropical embayment: implications for resource partitioning. Mar Biol 144:439–448. https://doi.org/10.1007/s00227-003-1218-1
Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JBC, Lotze HK, Michelli F, Palumbi SR, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790. https://doi.org/10.1126/science.1132294
Worm B, Davis B, Kettemer L, Ward-Paige CA, Demian C, Heithaus MR, Kessel ST, Gruber SH (2013) Global catches, exploitation rates, and rebuilding options for sharks. Mar Policy 40:194–204. https://doi.org/10.1016/j.marpol.2012.12.034
Zeichner SS, Colman AS, Koch PL, Polo-Silva C, Galván-Magaña F, Kim SL (2017) Discrimination factors and incorporation rates for organic matrix in shark teeth based on a captive feeding study. Physiol Biochem Zool 90:257–272. https://doi.org/10.1086/689192
Zenteno L, Borella F, Otero JG, Piana E, Belardi JB, Borrero LA, Saporiti F, Cardona L, Crespo E (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
We would like to thank the National Geographic Society (#EC-400R-18) for the funding that was vital to this study. Thanks to CAPES for the master’s degree scholarship; to the post-graduate ecology program (PPGECO-UFSC); to Jules M.R. Soto and Bibiana C. Lessa from the Univali Oceanographic Museum (MOVI), for welcoming us into the Museum’s space and providing samples for this study; to Maria C. Oddone and to the late Carolus M. Vooren from the Federal University of Rio Grande, for welcoming us into their labs and providing samples for this study; to Simon-Pierre Gilson and Luciane Scherer, for welcoming us to the research center of the Museum of Archeology and Ethnology at UFSC and for their help. We thank Karla Scherer for welcoming her into her workspace and hel** on countless occasions. We would also like to thank the UFSC multi-user laboratory, LAMEB. Finally, we would like to thank Clarissa Teixeira and Luiza Pereira for their guidance in the world of stable isotopes.
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This research was funded through National Geographic Society, early career grant, of number EC-400R-18.
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GBM: conceived the study and designed the experiments. Material preparation and data collection were performed by all the authors. Data analysis was performed by GBM. The first draft of the manuscript was written by GBM and RHAdF: revised and commented on previous versions of the manuscript. All the authors helped with funding acquisition. All the authors read and approved the final manuscript.
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Burg Mayer, G., de Freitas, R.H.A. Archaeological sharks: changes in the trophic ecology between late Holocene and modern shark communities in South Brazil. Mar Biol 170, 102 (2023). https://doi.org/10.1007/s00227-023-04252-x
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DOI: https://doi.org/10.1007/s00227-023-04252-x