Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-26T02:55:04.494Z Has data issue: false hasContentIssue false
  • English
  • Français

Use of stable isotopes in the evaluation of fish trophic guilds from a tropical hypersaline lagoon

Published online by Cambridge University Press:  29 October 2020

Marcos A. L. Franco Open the ORCID record for Marcos A. L. Franco [Opens in a new window] ,
Alejandra F. G. N. Santos ,
Abílio S. Gomes ,
Marcelo G. de Almeida  and
Carlos E. de Rezende
Marcos A. L. Franco*
Affiliation:
Universidade Estadual do Norte Fluminense (UENF), Centro de Biociências e Biotecnologia, Laboratório de Ciências Ambientais, Av. Alberto Lamego, 2000, Horto, CEP: 28013-602, Campos dos Goytacazes, Rj, Brazil
Alejandra F. G. N. Santos
Affiliation:
Universidade Federal Fluminense (UFF), Laboratory of Applied Ecology, Rua Vital Brazil Filho, 64, CEP: 24230-340, Niterói, Rj, Brazil
Abílio S. Gomes
Affiliation:
Universidade Federal Fluminense (UFF), Laboratory of Applied Ecology, Rua Vital Brazil Filho, 64, CEP: 24230-340, Niterói, Rj, Brazil
Marcelo G. de Almeida
Affiliation:
Universidade Estadual do Norte Fluminense (UENF), Centro de Biociências e Biotecnologia, Laboratório de Ciências Ambientais, Av. Alberto Lamego, 2000, Horto, CEP: 28013-602, Campos dos Goytacazes, Rj, Brazil
Carlos E. de Rezende
Affiliation:
Universidade Estadual do Norte Fluminense (UENF), Centro de Biociências e Biotecnologia, Laboratório de Ciências Ambientais, Av. Alberto Lamego, 2000, Horto, CEP: 28013-602, Campos dos Goytacazes, Rj, Brazil
*
Author for correspondence: Marcos A. L. Franco, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Environmental factors, size-related isotopic changes of the most abundant species and isotopic niche overlap were investigated using stable isotopes in order to evaluate spatial changes of fish trophic guilds in the Araruama Lagoon. Based on 440 muscle samples, 17 fish species were grouped into five trophic guilds. Mean salinity was above 40 at both sites sampled and a significant spatial difference was observed. The highest δ13C mean value was observed for an omnivorous species, whereas the lowest carbon signatures were found for the three fish species belonging to the planktivorous guild. Analysis of the carbon signature of fish species in lower trophic levels showed influence of salinity variation, whilst size appeared to play a role for others. A narrow δ15N difference was observed, but the piscivorous fish species showed the highest δ15N values. The Standard Ellipses Analysis (SEA) detected spatial differences and varying degrees of isotopic niche overlap among trophic guilds, but the percentages of most overlaps (<60%) suggest that, to some extent, the guilds had a unique isotopic niche space. These results are in agreement with data previously reported for the Araruama Lagoon, that found the same prey items with varying relative importance among the most abundant species. Further studies are necessary to understand how the interaction between salinity and other factors, such as migration patterns, changes in prey availability, changes in contribution of primary sources and changes in baseline isotopic signatures could affect the stable isotope signatures shown here.

Keywords

Carbonhypersaline lagoonnitrogentrophic guilds
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 100 , Issue 6 , September 2020 , pp. 979 - 988
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Almeida-Silva, PH, Tubino, RA, Zambrano, LC, Hunder, DA, Garritano, SR and Monteiro-Neto, C (2015) Trophic ecology and food consumption of fishes in a hypersaline tropical lagoon. Journal of Fish Biology 86, 1781–1795.10.1111/jfb.12689CrossRefGoogle Scholar
André, DL, Oliveira, MC, Okuda, T, Horta, AMTC, Soldan, AL, Moreira, IMNS, Rollemberg, MCE and Heinzen, VEF (1981) Estudo preliminar sobre as condições hidroquímicas da lagoa de Araruama, Rio de Janeiro. Instituto de Pesquisas da Marinha 139, 1–35.Google Scholar
Barbieri, EB (1975) Ritmo climático e extraçao do sal em Cabo Frio. Revista brasileira de Geografia 37, 23–109.Google Scholar
Bearhop, S, Adams, CE, Waldron, S, Fuller, RA and Macleod, H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology 73, 1007–1012.10.1111/j.0021-8790.2004.00861.xCrossRefGoogle Scholar
Bidegain, P and Bizerril, C (2002) Lagoa de Araruama. Perfil Ambiental do maior ecossistema lagunar hipersalino do mundo. Semads, Rio de Janeiro.Google Scholar
Bintz, JC, Nixon, SW, Buckley, BA and Granger, SL (2003) Impacts of temperature and nutrients on coastal lagoon plant communities. Estuaries 26, 765–776.10.1007/BF02711987CrossRefGoogle Scholar
Bouillon, S, Connolly, RM and Gillikin, DP (2011) Use of stable isotopes to understand food webs and ecosystem functioning in estuaries. In Wolanski, E and McLusky, DS (eds), Treatise on Estuarine and Coastal Science, vol. 7. Waltham, MA: Academic Press, pp. 143–173.10.1016/B978-0-12-374711-2.00711-7CrossRefGoogle Scholar
Braga, CZF, Vianna, ML and Kjerfve, B (2003) Environmental characterization of a hypersaline coastal lagoon from Landsat-5 Thematic Mapper data. International Journal of Remote Sensing 24, 3219–3234.10.1080/0143116031000075099CrossRefGoogle Scholar
Bruno, DO, Barbini, SA, Astarloa, JMD and Martos, P (2013) Fish abundance and distribution patterns related to environmental factors in a choked temperate coastal lagoon (Argentina). Brazilian Journal of Oceanography 61, 43–53.10.1590/S1679-87592013000100005CrossRefGoogle Scholar
Clementino, MM, Vieira, RP, Cardoso, AM, Nascimento, APA, Silveira, CB, Riva, TC, Gonzalez, ASM, Paranhos, R, Albano, RM, Ventosa, A and Martins, OB (2008) Prokaryotic diversity in one of the largest hypersaline coastal lagoons in the world. Extremophiles 12, 595–604.10.1007/s00792-008-0162-xCrossRefGoogle Scholar
Cruz, LR, Santos, LN and Santos, AFGN (2018) Changes of fish trophic guilds in Araruama Lagoon, Brazil: what can be inferred about functioning and structure of hypersaline lagoons? Estuarine Coastal and Shelf Science 211, 90–99.10.1016/j.ecss.2017.11.024CrossRefGoogle Scholar
Davias, LA, Kornis, MS and Breitburg, DL (2013) Environmental factors influencing δ13C and δ15N in three Chesapeake Bay fishes. ICES Journal of Marine Science 71, 689–702.10.1093/icesjms/fst143CrossRefGoogle Scholar
Deegan, BM, Lamontagne, S, Aldridge, KT and Brookes, JD (2010) Trophodynamics of the Coorong. Spatial Variability in Food Web Structure Along a Hypersaline Coastal Lagoon. Glen Osmond: CSIRO.Google Scholar
Doi, H, Zuykova, EI, Shikano, S, Kikuchi, E, Ota, H, Yurlova, NI and Yandrenkina, E (2013) Isotopic evidence for the spatial heterogeneity of the planktonic food webs in the transition zone between river and lake ecosystems. PeerJ 1, e222. doi: 107717/peerj.222Google ScholarPubMed
Fry, B (2002) Conservative mixing of stable isotopes across estuarine salinity gradients: a conceptual framework for monitoring watershed influences on downstream fisheries production. Estuaries 25, 265–271.10.1007/BF02691313CrossRefGoogle Scholar
Gilikin, DP, Lorrain, A, Bouillon, S, Willenz, P and Dehairs, F (2006) Stable carbon isotopic composition of Mytilus edulis shells: relation to metabolism, salinity, δ13CDIC and phytoplankton. Organic Chemistry 37, 1371–1382.Google Scholar
Hair, JF, Anderson, RE, Tatham, L and Grablowski, BJ (1984) Multivariate Data Analysis. New York, NY: Macmillan.Google Scholar
Harrod, C, Grey, J, McCarthy, TK and Morrissey, M (2005) Stable isotope analyses provide new insights into ecological plasticity in a mixohaline population of European eel. Oecologia 144, 673–683.10.1007/s00442-005-0161-xCrossRefGoogle Scholar
Houssain, MA, Ye, Q, Leterme, SC and Qin, JG (2016) Spatial and temporal changes of three prey-fish assemblage structure in a hypersaline lagoon: the Coroong, South Australia. Marine and Freshwater Research 68, 282–292.10.1071/MF15212CrossRefGoogle Scholar
IBGE (2018) Available at www.cidades.igbe.gov.br (Accessed 24 March 2018).Google Scholar
Jackson, AL, Inger, R, Parnell, AC and Bearhop, S (2011) Comparing isotopic niche widths among and within communities: SIBER – Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80, 595–602.10.1111/j.1365-2656.2011.01806.xCrossRefGoogle ScholarPubMed
Kilujen, M, Grey, J, Sinisalo, T, Harrod, C, Immonen, H and Jones, RI (2006) A revised model for lipid-normalizing δ13C values from aquatic organisms, with implications for isotope mixing models. Journal of Applied Ecology 43, 1213–1222.10.1111/j.1365-2664.2006.01224.xCrossRefGoogle Scholar
Kjerfve, B (1986) Comparative oceanography of coastal lagoons. In Wolfe, DA (ed.), Estuarine Variability. New York, NY: Academic Press, pp. 63–81.10.1016/B978-0-12-761890-6.50009-5CrossRefGoogle Scholar
Kjerfve, B, Schettini, CA, Knoppers, B, Lessa, G and Ferreira, HO (1996) Hydrology and salt balance in a large, hypersaline coastal lagoon: Lagoa de Araruama, Brazil. Estuarine Coastal and Shelf Science 42, 701–725.10.1006/ecss.1996.0045CrossRefGoogle Scholar
Layman, CA, Arrington, DA, Montaña, CG and Post, DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88, 42–48.10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2CrossRefGoogle ScholarPubMed
Litvin, SY and Weinstein, MP (2004) Multivariate analysis of stable-isotope ratios to infer movements and utilization of estuarine organic matter by juvenile weakfish (Cynoscion regalis). Canadian Journal of Fisheries and Aquatic Sciences 61, 1851–1861.Google Scholar
Martinelli, LA, Ometto, JPHB, Ferraz, ES, Victoria, RL, Camargo, PB and Moreira, MZ (2009) Desvendando questões ambientais com isótopos estáveis. São Paulo: Oficina de textos, 144 pp.Google Scholar
Mont'Alverne, R, Pereyra, PE and Garcia, AM (2016) Trophic segregation of a fish assemblage along lateral depth gradients in a subtropical coastal lagoon revealed by stable isotope analyses. Journal of Fish Biology 89, 770–792.10.1111/jfb.12903CrossRefGoogle Scholar
Moreira-Turcq, PF (2000) Impact of a low salinity year on the metabolism of a hypersaline coastal lagoon (Brazil). Hydrobiologia 429, 133–140.10.1023/A:1004037624787CrossRefGoogle Scholar
Moreno, IM, Ávila, A and Losada, MA (2010) Morphodynamics of intermittent coastal lagoons in Southern Spain: Zahara de los Atunes. Geomorphology 121, 305–316.10.1016/j.geomorph.2010.04.028CrossRefGoogle Scholar
Mouillot, D, Gaillard, S, Aliaume, C, Verlaque, M, Belsher, T, Troussellier, M and Do Chi, T (2005) Ability of taxonomic diversity indices to discriminate coastal lagoon environments based on macrophyte communities. Ecological Indicators 5, 1–17.10.1016/j.ecolind.2004.04.004CrossRefGoogle Scholar
Muro-Torres, VM, Soto-Jimenéz, MF, Green, L, Quintero, J and Amezcua, F (2019) Food web structure of a subtropical coastal lagoon. Aquatic Ecology 53, 407–430.10.1007/s10452-019-09698-0CrossRefGoogle Scholar
Newsome, SD, Rio, CM, Bearhop, S and Phillips, DL (2007) A niche for isotopic ecology. Frontiers in Ecology and the Environment 5, 429–436.10.1890/1540-9295(2007)5[429:ANFIE]2.0.CO;2CrossRefGoogle Scholar
O'Farrell, S, Bearhop, S, McGill, RAR, Dahlgren, CP, Brumbaugh, DR and Mumby, PJ (2014) Habitat and body size effects on the isotopic niche space of invasive lionfish and endangered Nassau grouper. Ecosphere (Washington, D.C.) 5, 123–133.Google Scholar
Peterson, BJ and Fry, B (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology, Evolution, and Systematics 18, 293–320.10.1146/annurev.es.18.110187.001453CrossRefGoogle Scholar
Post, DM (2002) Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83, 703–718.10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2CrossRefGoogle Scholar
PROLAGOS (2016) Available at www.prolagos.com.br (Accessed 24 March 2018).Google Scholar
Rakhesh, M, Madhavirani, KSVKS, Charan-Kumar, B, Raman, AV, Kalavati, C, Prabhakara Rao, Y, Rosamma, S, Ranga Rao, V, Gupta, GVM and Subramanian, BR (2015) Trophic-salinity gradients and environmental redundancy resolve mesozooplankton dynamics in a large tropical coastal lagoon. Regional Studies in Marine Science 1, 72–84.10.1016/j.rsma.2015.04.003CrossRefGoogle Scholar
R Core Team (2017) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Root, RB (1967) The niche exploitation pattern of the blue-gray gnatcatcher. Ecological Monographs 37, 317–350.10.2307/1942327CrossRefGoogle Scholar
Rosa, JCL, Alberto, MD, Ribas, WMM, Neves, MHCB and Fernandes, LDA (2016) Spatial variability in the icthyoplankton structure of a subtropical hypersaline lagoon. Brazilian Journal of Oceanography 64, 149–156.10.1590/S1679-87592016109406402CrossRefGoogle Scholar
Saad, AM (2003) Composição, distribuição especial, dinâmica de populações de peixes e estatística pesqueira na lagoa hipersalina de Araruama, RJ. PhD thesis, Universidade Federal de São Carlos.Google Scholar
Sánchez-Hernández, J, Elloranta, AP, Finstad, AG and Amundsen, PA (2017) Community structure affects trophic ontogeny in a predatory fish. Ecology and Evolution 7, 358–367.10.1002/ece3.2600CrossRefGoogle Scholar
Shaw, AL, Frazier, BS, Kucklick, JR and Sancho, G (2016) Trophic ecology of a predator community in a shallow-water, high-salinity estuary assessed by stable isotope analysis. Marine and Coastal Fisheries 8, 46–61.10.1080/19425120.2015.1121940CrossRefGoogle Scholar
Simberloff, D and Dayan, T (1991) The guild concept and the structure of ecological communities. Annual Review of Ecology, Evolution, and Systematics 22, 115–143.10.1146/annurev.es.22.110191.000555CrossRefGoogle Scholar
Slack-Smith, RJ, Faria, FOS, Jablonski, S and Rodrigues, LF (1977) Camarão-Rosa (Penaeus brasiliensis Latreille) na Lagoa de Araruama, Rio de Janeiro – 1ª Parte: Resultados de amostragens de capturas e análises da pesca artesanal. SUDEPE/PDP, Série Documentos Técnicos, No. 22, 53 pp.Google Scholar
Souza, MFL, Kjerfve, B, Knoppers, BA, Landim, WF and Damasceno, RN (2003) Nutrient budgets and trophic state in a hypersaline coastal lagoon: Lagoa de Araruama, Brazil. Estuarine, Coastal and Shelf Science 57, 843–858.10.1016/S0272-7714(02)00415-8CrossRefGoogle Scholar
Vegas-Sandejas, ME and Santillana, MH (2004) Fish community structure and dynamics in a coastal hypersaline lagoon: Rio Lagartos, Yucatan, Mexico. Estuarine, Coastal and Shelf Science 60, 285–299.10.1016/j.ecss.2004.01.005CrossRefGoogle Scholar
Vizzini, S and Mazzola, A (2008) The fate of organic matter sources in coastal environments: a comparison of three Mediterranean lagoons. Hydrobiologia 611, 67–79.10.1007/s10750-008-9458-1CrossRefGoogle Scholar