Skip to main content
SpringerLink
Log in

Genetics and stable isotopes reveal non-obvious population structure of bottlenose dolphins (Tursiops truncatus) around the Balearic Islands

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The effective management of wildlife requires that populations are defined in a biological sensible manner. We investigated the population structure of bottlenose dolphins (Tursiops truncatus) in waters around the Balearic archipelago using two complementary techniques; DNA markers (i.e. microsatellites and a portion of the mitochondrial control region) and stable isotopes (δ13C, δ15N). We used tissue samples from biopsies (n = 50) and fresh carcasses (n = 7) obtained around the islands of Gimnèsies and Pitiüses, and Comunitat Valenciana (Western Mediterranean Sea). Genetic differentiation between individuals from Gimnésies and Pitiüses and between individuals from across these two areas and individuals from Comunitat Valenciana was significant when assessing FST, but no substructure was found using clustering methods (i.e. DAPC and Bayesian clustering). δ13C and δ15N profiles were not significantly different between dolphins from Gimnésies and Pitiüses. Dolphins from both areas showed coastal carbon isotopic values and similar trophic niche levels. However, the trophic niche of dolphins from Gimnésies was broader than the trophic niche of Pitiüses’ dolphins. These results indicate non-obvious population structure between the mainland and the archipelago, or between islands within the archipelago. The use of combined techniques, which integrate information over different time scales, is applicable to other species and areas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abelson, P. H. & T. C. Hoering, 1961. Carbon isotope fractionation in formation of amino acids by photosynthetic organisms. Proceedings of the National Academy of Sciences United States of America 47(5): 623–632.

    Article  CAS  Google Scholar 

  • Anderson, M. J., R. N. Gorley & K. R. Clarke, 2008. PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth.

    Google Scholar 

  • ASCOBANS, 2009. Report of ASCOBANS/HELCOM small cetacean population structure workshop. In EvP. G. H. & J. Teilman (eds), ASCOBANS, Bonn, Germany.

  • Bearzi, G. & C. M. Fortuna, 2006. Common bottlenose dolphin Tursiops truncatus (Meditarranean subpopulation). In Reeves, R. R. & G. Notarbartolo-di-Sciara (eds), The Status and Distribution of Cetaceans in the Black Sea and Mediterranean Sea. UICN Centre for Mediterranean Cooperation, Málaga: 64–73.

    Google Scholar 

  • Bearzi, G., E. Politi, S. Agazzi, S. Bruno, M. Costa & S. Binizzoni, 2005. Occurrence and present status of coastal dolphins (Delphinus delphis and Tursiops truncatus) in the eastern Ionian Sea. Aquatic Conservation Marine and Freshwater Ecosystems 15: 243–257.

    Article  Google Scholar 

  • Bearzi, G., D. Holcer & G. Notarbartolo-di-Sciara, 2004. The role of historical dolphin takes and habitat degradation in shaping the present status of northern Adriatic cetaceans. Aquatic Conservation Marine and Freshwater Ecosystems 14: 363–379.

    Article  Google Scholar 

  • Begg, G. A., K. D. Friedland & J. B. Pearce, 1999. Stock identification and its role in stock assessment and fisheries management: an overview. Fisheries Research 43(1–3): 1–8.

    Article  Google Scholar 

  • Blanco, C., O. Salomon & J. A. Raga, 2001. Diet of bottlenose dolphin (Tursiops truncatus) in the western Mediterranean sea. Journal of the Marine Biological Association of the United Kingdom 81: 1053–1058.

    Article  Google Scholar 

  • Blanco, J. C. & J. L. González, 1992. Libro Rojo de los Vertebrados de España. Ministerio de Agricultura, Pesca y Alimentación, ICONA, Madrid.

    Google Scholar 

  • Borrell, A., A. Aguilar, J. Forcada, M. Fernández, F. J. Aznar & J. A. Raga, 2000. Varamiento de cetáceos en las costas españolas del Mediterráneo durante el periodo 1989–1992. Miscellània Zoològica 23: 53–69.

    Google Scholar 

  • Borrell, A., A. Aguilar, V. Tornero, M. Sequeiro, G. Fernández & S. Alis, 2006. Organochlorine compounds and stable isotopes indicate bottlenose dolphin subpopulation around the Iberian Peninsula. Environment International 32: 516–523.

    Article  CAS  PubMed  Google Scholar 

  • Box, A., S. Deudero, A. Blanco, A. M. Grau & F. Riera, 2010. Differences in δ13C and δ15N stable isotopes in the pearly razorfish Xyrichtys novacula related to the sex, location and spawning period. Journal of Fish Biology 76: 2370–2381.

    Article  CAS  PubMed  Google Scholar 

  • Brotons, J. M., A. M. Grau & L. Rendell, 2008. Estimating the impact of interactions between bottlenose dolphins and artisanal fisheries around the Balearic Islands. Marine Mammal Science 24(1): 112–127.

    Article  Google Scholar 

  • Cadrin, S., L. Kerr & S. Mariani, 2013. Stock Identification Methods: Applications in Fishery Science, 2nd ed. Elsevier, Amsterdam.

    Google Scholar 

  • Capelli, R., K. Das, R. De Pellegrini, G. Drava, G. Lepoint, C. Miglio, V. Minganti & R. Poggi, 2008. Distribution of trace elements in organs of six species of cetaceans from the Ligurian Sea (Mediterranean), and the relationship with stable carbon and nitrogen ratios. Science of the Total Environment 390(2–3): 569–578.

    Article  CAS  Google Scholar 

  • Cardona, L., M. Revelles, M. Sales, A. Aguilar & A. Borrell, 2007. The meadows of the seagrass Posidonia oceanica are a relevant source of organic matter for adjoining ecosystems. Marine Ecology Progress Series 335: 123–131.

    Article  CAS  Google Scholar 

  • Cherel, Y. & K. A. Hobson, 2007. Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Marine Ecology Progress Series 329: 281–287.

    Article  CAS  Google Scholar 

  • Chilvers, B. L. & P. J. Corkeron, 2001. Trawling and bottlenose dolphin’s social structure. Proceedings of the Royal Society of London B 268: 1901–1905.

    Article  CAS  Google Scholar 

  • Chouvelon, T., J. Spitz, F. Caurant, P. Méndez, A. Chappuis, F. Laugier, E. Le Goff & P. Bustamante, 2012. Revisiting the use of δ15N in meso-scale studies of marine food webs by considering spatio-temporal variations in stable isotopic signatures. The case of an open ecosystem: the Bay of Biscay (north-east Atlantic). Progress in Oceanography 101: 95–102.

    Article  Google Scholar 

  • Clement, M., D. Posada & K. A. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659.

    Article  CAS  PubMed  Google Scholar 

  • Donaldson, R., H. Finn, L. Bejder, D. Lusseau & M. Calver, 2012. The social side of human-wildlife interaction: wildlife can learn harmful behaviours from each other. Animal Conservation 15: 427–435.

    Article  Google Scholar 

  • Durand, E., C. Chen. & O. François, 2009. Tess Version 2.1—Reference Manual. http://membrestimc.imag.fr/Olivier.Francois/tess.html.

  • Earl, D. A. & B. M. vonHoldt, 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4(2): 359–361.

    Article  Google Scholar 

  • Evanno, G., S. Regnaut, and J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14(8): 2611–2620.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L., and H. E. L. Lischer, 2010. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  PubMed  Google Scholar 

  • Fantle, M. S., A. I. Dittel, S. M. Schwalm, C. E. Epifanio & M. L. Fogel, 1999. A food web analysis of the juvenile blue crab, Callinectes sapidus, using stable isotopes in whole animals and individual amino acids. Oecologia 120: 416–426.

    Article  PubMed  Google Scholar 

  • Fernández, R., S. García-Tiscar, M. B. Santos, A. López, J. A. Martínez-Cedeira, J. Newton & G. J. Pierce, 2011. Stable isotope analysis in two sympatric populations of bottlenose dolphins Tursiops truncatus: evidence of resource partitioning? Marine Biology 158: 1043–1055.

    Article  Google Scholar 

  • Folch, J., M. Lees & G. H. S. Stanley, 1957. A simple method for the isolation and purification of total lipids from animal tissues. The Journal of Biological Chemistry 226: 497–509.

    CAS  PubMed  Google Scholar 

  • Foote, A. D., J. Newton, S. B. Piertney, E. Willerslev & T. M. Gilbert, 2009. Ecological, morphological and genetic divergence of sympatric North Atlantic killer whale populations. Molecular Ecology 18(24): 5207–5217.

    Article  CAS  PubMed  Google Scholar 

  • García-Tiscar, S., 2010. Interacciones entre delfines mulares (Tursiops truncatus), orcas (Orcinus orca) y pesquerías en el Mar de Alborán y el estrecho de Gibraltar. PhD Thesis, Universidad Autónoma de Madrid.

  • Gaspari, S., A. Scheinin, D. Holcer, C. M. Fortuna, C. Natali, T. Genov, A. Frantzis, G. Chelazzi & A. E. Moura, 2015. Drivers of population structure of the bottlenose dolphin (Tursiops truncatus) in the Eastern Mediterranean Sea. Evolutionary Biology 42: 177–190.

    Article  Google Scholar 

  • Gazo, M., J. Gonzalvo & A. Aguilar, 2008. Pingers as deterrents of bottlenose dolphins interacting with trammel nets. Fisheries Research 92: 70–75.

    Article  Google Scholar 

  • Gibbs, S. E., R. G. Harcourt & C. M. Kemper, 2011. Niche differentiation of bottlenose dolphin species in South Australia revealed by stable isotopes and stomach contents. Wildlife Resecrah 38(4): 261–270.

    Article  CAS  Google Scholar 

  • Giménez, J., F. Ramirez, J. Almunia, M. G. Forero & R. Stephanis, 2016. From the pool to the sea: applicable isotope turnover rates and diet to skin discrimination factors for bottlenose dolphins (Tursiops truncatus). Journal of Eperimental Marine Biology and Ecology 475: 54–61.

    Article  CAS  Google Scholar 

  • Giménez, J., A. Marçalo, F. Ramírez, P. Verborgh, P. Gauffier, R. Esteban & J. Vingada, 2017a. Diet of bottlenose dolphins (Tursiops truncatus) from the Gulf of Cadiz: insights from stomach content and stable isotope analyses. PLoS ONE 12(9): e0184673.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giménez, J., F. Ramírez, M. G. Forero, J. Almunia, R. de Stephanis & J. Navarro, 2017b. Lipid effects on isotopic values in bottlenose dolphins (Tursiops truncatus) and their prey with implications for diet assessment. Marine Biology 164(6): 122.

    Article  CAS  Google Scholar 

  • Giménez, J., M. Louis, E. Barón, F. Ramírez, P. Verborgh, P. Gauffier & R. Stephanis, 2018. Towards the identification of ecological management units: a multidisciplinary approach for the effective management of bottlenose dolphins in the southern Iberian Peninsula. Aquatic Conservation: Marine and Freshwater Ecosystems 28(1): 205–215.

    Article  Google Scholar 

  • Gonzalvo, J., J. Forcada, E. Grau & A. Aguilar, 2014. Strong site-fidelity increases vulnerability of common bottlenose dolphins Tursiops truncatus in a mass tourism destination in the western Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom 94(6): 1227–1235.

    Article  Google Scholar 

  • Goudet, J., 1995. FSTAT (version 1.2): A computer program to calculate F-statistics. Journal of the Heredity 86(6): 485–486.

    Article  Google Scholar 

  • Guillot, G., 2009. On the inference of spatial structure from population genetics data. Bioinformatics 25: 1796–1801.

    Article  CAS  PubMed  Google Scholar 

  • Hobson, K. A., W. G. Ambrose & P. E. Renaud, 1995. Sources of primary production, benthic-pelagic coupling, and trophic relationships within the Northeast Water Polynya: insights from δ13C and δ15N analysis. Marine Ecology Progress Series 128(1–3): 1–10.

    Article  Google Scholar 

  • Jackson, A. L., R. Inger, A. C. Parnell & S. Bearhop, 2011. Comparing isotopic niche widths among and within communities: SIBER – stable isotope Bayesian ellipses in R. Journal of Animal Ecology 80: 595–602.

    Article  Google Scholar 

  • Jombart, T., 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405.

    Article  CAS  PubMed  Google Scholar 

  • Kopps, A. M., C. Y. Ackermann, W. B. Sherwin, S. J. Allen, L. Bejder & M. Krützen, 2014. Cultural transmission of tool use combined with habitat specializations leads to fine-scale genetic structure in bottlenose dolphins. Proceedings of the Royal Society series B 281: 20133245.

    Article  Google Scholar 

  • Krützen, M., J. Mann, M. R. Heithaus, R. C. Connor, L. Bejder & W. B. Sherwin, 2005. Cultural transmission of tool use in bottlenose dolphins. PNAS 201(25): 8939–8943.

    Article  CAS  Google Scholar 

  • Latch, E. K., G. Dharmarajan, J. C. Glaubitz & O. E. J. Rhodes, 2006. Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conservation Genetics 7: 295.

    Article  Google Scholar 

  • Layman, C. A., D. A. Arrington, C. G. Montañna & D. M. Post, 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88(1): 42–48.

    Article  PubMed  Google Scholar 

  • Louis, M., M. C. Fontaine, J. Spitz, E. Schlund, W. Dabin, R. Deaville & B. Simon-Bouhet, 2014a. Ecological opportunities and specializations shaped genetic divergence in a highly mobile marine top predator. Proceedings of the Royal Society Series B 281(1795): 20141558.

    Article  Google Scholar 

  • Louis, M., A. Viricel, T. Lucas, H. Peltier, E. Alfonsi, S. Berrow, A. Brownlow, P. Covelo, W. Dabin, R. Deaville, R. De Stephanis, F. Gally, P. Gauffier, R. Penrose, M. A. Silva, C. Guinet & B. Simon-Bouhet, 2014b. Habitat-driven population structure of bottlenose dolphins, Tursiops truncatus, in the North-East Atlantic. Molecular Ecology 23(4): 857–874.

    Article  PubMed  Google Scholar 

  • Miokovic, D., D. Kovacic & S. Pribanic, 1999. Stomach content analysis of one bottlenose dolphin (Tursiops truncatus, Montagu, 1821) from the Adriatic Sea. Natura Croatia 8: 61–65.

    Google Scholar 

  • Morin, Y. & V. Lesage V, 2003. Effects of DMSO and lipid extraction methods on stable carbon and nitrogen isotopes ratios in the skin of odontocetes and mysticetes. Proceedings of the 15th biennial conference on the biology of marine mammals, 14–19 December, Greensboro, North Carolina, USA.

  • Natoli, A., A. Birkun, A. Aguilar, A. López & A. R. Hoelzel, 2005. Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus). Proceedings of the Royal Society of London B 272: 1217–1226.

    Article  CAS  Google Scholar 

  • Newsome, S. D., M. T. Clementz, and P. L. Koch, 2010. Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science 26(3): 509–572.

    CAS  Google Scholar 

  • Ozerov, M. M., P. V. Himberg, H. Hägerstrand Debes & A. Vasemägi, 2016a. Combining genetic markers with an adaptive meristic trait improves performance of mixed-stock analysis in Baltic whitefish. ICES Journal of Marine Science 73(10): 2529–2538.

    Article  Google Scholar 

  • Ozerov, M. Y., M. Himberg, P. V. Debes, H. Hägerstrand & A. Vasemägi, 2016b. Combining genetic markers with an adaptive meristic trait improves performance of mixed-stock analysis in Baltic whitefish. ICES Journal of Marine Science 73(10): 2529–2538.

    Article  Google Scholar 

  • Parnell A. C. & A. L. Jackson, 2013. SIAR: Stable Isotope Analysis in R. R package version 4.2 (https://CRAN.R-project.org/package=siar).

  • Payo-Payo, A., B. Ruiz, L. Cardona & A. Borrell, 2013. Effects of tissue decomposition on stable isotope signatures of striped dolphins Stenella coeruleoalba and loggerhead sea turttles Caretta caretta. Aquatic Biology 18: 141–147.

    Article  Google Scholar 

  • Peterson, B. J. & B. Fry, 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology, Evolution, and Systematics 18: 293–320.

    Article  Google Scholar 

  • Pritchard, J. K., M. Stephens, and P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155(2): 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pryor, K., J. Lindbergh, S. Lindbergh & R. Milano, 1990. A dolphin-human fishing cooperative in Brazil. Marine Mammal Science 6: 77–82.

    Article  Google Scholar 

  • Queller, D. C. & K. F. Goodnight, 1989. Estimating relatedness using genetic markers. Evolution 43: 258–275.

    Article  PubMed  Google Scholar 

  • Quérouil, S., M. Silva, L. Freitas, S. Magalhães, A. Dinis, F. Alves, J. Matos, D. Mendonça, P. Hammond & R. Santos, 2007. High gene flow in oceanic bottlenose dolphins (Tursiops truncatus) of the North Atlantic. Conservation Genetics 8: 1405–1419.

    Article  CAS  Google Scholar 

  • Rau, G. H., D. G. Ainley, J. L. Bengtson, J. J. Torres & T. L. Hopkins, 1992. 15N/14N and 13C/12C in Weddell Sea birds, seals, and fish: implications for diet and trophic structure. Marine Ecology Progress Series 84: 1–8.

    Article  CAS  Google Scholar 

  • Raymond, M. & F. Rousset, 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of the Heredity 86: 248–249.

    Article  Google Scholar 

  • Reeves, R. R., and G. Notarbartolo Di Sciara, 2006. The status and distribution of cetaceans in the Black Sea and Mediterranean Sea. Malaga, Spain: IUCN Centre for Mediterranean Cooperation.

    Google Scholar 

  • Reis-Santos, P., S. E. Tanner, S. França, R. P. Vasconcelos, B. M. Gillanders & H. N. Cabral, 2015. Connectivity within estuaries: an otolith chemistry and muscle stable isotope approach. Ocean and Coastal Management 118: 51–59.

    Article  Google Scholar 

  • Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.

    Article  PubMed  Google Scholar 

  • Rosel, P. E., 2003. PCR-based sex determination in Odontocete cetaceans. Conservation genetics 4(5): 647–649.

    Article  CAS  Google Scholar 

  • Smith, R. J., K. A. Hobson, H. N. Koopman & D. M. Lavigne, 1996. Distinguishing between populations of fresh- and salt water harbour seals (Phoca vitulina) using stable-isotope ratios and fatty acid profiles. Canadian Journal of Fisheries and Aquatic Sciences 53: 272–279.

    Article  Google Scholar 

  • Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills, and P. Shipley, 2004. Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology notes 4(3): 535–538.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study has been financially supported by FEP (Fondo Europeo de Pesca) European funds. Obtaining biopsies would have been impossible without the excellent work of Alex, Jorge, Yann, Santi and Tomeu, from the surveillance team of the marine reserves of the DGMRM (Direcció General de Medi Rural i Marí) in the Balearic Islands and E. Minués, J. Jiménez, and the Serra Gelada reserve’s staff in the Comunitat Valenciana. P. Gozalbes and T. Raga from the University of Valencia provided us selflessly with samples from strandings. The support by the DGMRM has been essential for the collection and analysis of data. Thanks to J.M. Valencia, M. Cerdá, E. Alvarez, A. M. Grau, and A. Frau for their help. The authors also thank the Scientist-Technical Services (University of the Balearic Islands) for collaboration in isotopic analysis and especially the support offered by B. Martorell. Many thanks for logistic support in preparing samples for isotopic analysis from P. Sarriera and F. Fuster and T. Amengual especially in the lipid extraction process. Authors thank M. Compa for assistance with the statistical R Programming Environment. Thanks to the two anonymous reviewers that contributed to an improved manuscript and to Dr. Alex Sansom for comments on the writing. Finally, thanks for the valuable supervision, support and generosity of Dr Luke Rendell.

Funding

This study was funded by FEP (Fondo Europeo de Pesca; Grant Number FEP 311NBAL00002).

Author information

Authors and Affiliations

  1. Direcció General de Medi Rural i Marí, Govern de les Illes Balears, Foners 10, 07006, Palma, Balearic Islands, Spain

    José M. Brotons

  2. Asociación Tursiops, c/Pop, 25 1er. 07639, Sa Ràpita, Balearic Islands, Spain

    José M. Brotons

  3. Sea Mammal Research Unit, Scottish Oceans Institute, University of St. Andrews, St. Andrews, Fife, KY16 8LB, UK

    Valentina Islas-Villanueva

  4. CONACYT Universidad del Mar, Cd. Universitaria, Puerto Ángel, San Pedro Pochutla, 70902, Oaxaca, Mexico

    Valentina Islas-Villanueva

  5. Instituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Moll de Ponent s/n, 07015, Palma, Balearic Islands, Spain

    Carme Alomar, Ariadna Tor & Salud Deudero

  6. International Council for the Exploration of the Sea (ICES), HC Andersens Boulevard 44-46, 1553, Copenhagen, Denmark

    Ruth Fernández

Authors
  1. José M. Brotons
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Valentina Islas-Villanueva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carme Alomar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ariadna Tor
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ruth Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Salud Deudero
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José M. Brotons.

Ethics declarations

Conflicts of interest

Author JMB declares that he has no conflict of interest. Author VI declares that she has no conflict of interest. Author CA declares that she has no conflict of interest. Author AT declares that she has no conflict of interest. Author RF declares that she has no conflict of interest. Author SD declares that she has no conflict of interest.

Additional information

Handling editor: Begoña Santos

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brotons, J.M., Islas-Villanueva, V., Alomar, C. et al. Genetics and stable isotopes reveal non-obvious population structure of bottlenose dolphins (Tursiops truncatus) around the Balearic Islands. Hydrobiologia 842, 233–247 (2019). https://doi.org/10.1007/s10750-019-04038-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-019-04038-7

Keywords

Search

Navigation