4.4 Perspectives
Our study highlights the applicability of
δ13CEAA fingerprinting in a regional
sea with strong salinity and temperature gradients by differentiating
among the trophic niches of both functional groups and species at an
unprecedented resolution, and by identifying spatial fingerprinting
differences of widely distributed species. These differences are likely
driven by regional differences in basal resources, i.e.
algal composition, and the
strength of trophic links between various phytoplankton producers and
consumers. Our study also highlights how CSIA can provide new insights
into food web structuring in spatially and temporally dynamic systems,
and thus complement traditional tools in trophic ecology, including
insights that are complementary to those from the “traditional” bulk
stable isotope analysis.
Current marine food webs are predicted to be fragile and susceptible to
structural changes with consequent alterations in the functioning of the
ecosystem (Marina et al. 2018). As environmental changes are
accelerating, it is crucial to understand whether and how quickly marine
food webs can adapt to changes in phytoplankton assemblages and
overexploitation of top predators. For this reason, it is key
identifying and quantifying feeding interactions across trophic levels,
from phytoplankton to zooplankton to higher trophic levels, but many of
these interactions remain crucial knowledge gaps (Griffiths et
al. 2017). The combination of δ13CEAAand the more affordable bulk stable isotope analysis holds considerable
promise to address these gaps in the future.
ACKNOWLEDGMENTS
We thank Dr. Nils Andersen, Karsten Gramenz and Robert Priester for
technical assistance at the Leibniz Laboratory for Isotope Research
(University of Kiel), and the scientific and permanent crew of RV Alkor
cruise AL476 for their support during fieldwork. The study was supported
by the Cluster of Excellence 80 ”The Future Ocean”, which is a framework
within the Excellence Initiative by the Deutsche Forschungsgemeinschaft
(DFG). Sampling on board of RV Alkor took place in the framework of the
BONUS BIO-C3 project. TL was supported by the Germany’s Federal Ministry
of Education and Research (BMBF) via LOMVIA (03V01459) and JD was in
part supported by the BONUS XWEBS project, both supported by BONUS (Art
185), funded jointly by the EU and the German BMBF. We declare no
conflict of interest.
CONFLICT OF INTEREST
None declared.
AUTHOR CONTRIBUTION
JD and TL conceived the study, JD collected the samples, TH determined
bulk isotope values, TL conducted amino acid isotope analyses and
performed statistical analysis, TL and JD wrote the manuscript, and all
authors commented on it.
DATA AVAILABILITY STATEMENT
Data associated with this paper are available in the Supplementary
Information.
References
Alheit, J., Möllmann, C., Dutz, J., Kornilovs, G., Loewe, P., Mohrholz,
V. & Wasmund, N. (2005) Synchronous ecological regime shifts in the
central Baltic and the North Sea in the late 1980s. Ices Journal
of Marine Science, 62, 1205-1215.
Anger, K., Rogal, U., Schriever, G. & Valentin, C. (1977) In-situ
investigations on the echinoderm Asterias rubens as a predator of
soft-bottom communities in the western Baltic Sea. Helgoländer
Wissenschaftliche Meeresuntersuchungen, 29, 439.
Armengol, L., Calbet, A., Franchy, G., Rodríguez-Santos, A. &
Hernández-León, S. (2019) Planktonic food web structure and trophic
transfer efficiency along a productivity gradient in the tropical and
subtropical Atlantic Ocean. Scientific Reports, 9, 2044.
Aro, E. (1988) Review of fish migration patterns in the Baltic Sea.
Bowser, A.K., Diamond, A.W. & Addison, J.A. (2013) From Puffins to
Plankton: A DNA-Based Analysis of a Seabird Food Chain in the Northern
Gulf of Maine. Plos One, 8, e83152.
Casini, M., Cardinale, M. & Arrhenius, F. (2004) Feeding preferences of
herring (Clupea harengus ) and sprat (Sprattus sprattus ) in
the southern Baltic Sea. Ices Journal of Marine Science,61, 1267-1277.
Casini, M., Käll, F., Hansson, M., Plikshs, M., Baranova, T., Karlsson,
O., Lundström, K., Neuenfeldt, S., Gårdmark, A. & Hjelm, J. (2016)
Hypoxic areas, density-dependence and food limitation drive the body
condition of a heavily exploited marine fish predator. Royal
Society open science, 3, 160416.
Cebrian, J. (1999) Patterns in the fate of production in plant
communities. The American Naturalist, 154, 449-468.
Chittenden, C.M., Ådlandsvik, B., Pedersen, O.P., Righton, D. &
Rikardsen, A.H. (2013) Testing a model to track fish migrations in polar
regions using pop‐up satellite archival tags. Fisheries
Oceanography, 22, 1-13.
Coplen, T.B. & Shrestha, Y. (2016) Isotope-abundance variations and
atomic weights of selected elements: 2016 (IUPAC Technical Report).Pure and Applied Chemistry, 88, 1203-1224.
Corr, L.T., Berstan, R. & Evershed, R.P. (2007) Development ofN -acetyl methyl ester derivatives for the determination of
δ13C values of amino acids using gas
chromatography-combustion-isotope ratio mass spectrometry.Analytical Chemistry, 79, 9082-9090.
Eero, M., Hjelm, J., Behrens, J., Buchmann, K., Cardinale, M., Casini,
M., Gasyukov, P., Holmgren, N., Horbowy, J. & Hüssy, K. (2015) Eastern
Baltic cod in distress: biological changes and challenges for stock
assessment. Ices Journal of Marine Science, 72,2180-2186.
Eglite, E., Graeve, M., Dutz, J., Wodarg, D., Liskow, I., Schulz‐Bull,
D. & Loick‐Wilde, N. (2019) Metabolism and foraging strategies of
mid‐latitude mesozooplankton during cyanobacterial blooms as revealed by
fatty acids, amino acids, and their stable carbon isotopes.Ecology and Evolution .
Elliott Smith, E.A., Harrod, C. & Newsome, S.D. (2018) The importance
of kelp to an intertidal ecosystem varies by trophic level: Insights
from amino acid δ13C analysis. Ecosphere,9, e02516.
Fry, B. (2006) Stable isotope ecology . Springer, New York.
Gasiūnaitė, Z.R., Cardoso, A.C., Heiskanen, A.S., Henriksen, P.,
Kauppila, P., Olenina, I., Pilkaitytė, R., Purina, I., Razinkovas, A.,
Sagert, S., Schubert, H. & Wasmund, N. (2005) Seasonality of coastal
phytoplankton in the Baltic Sea: Influence of salinity and
eutrophication. Estuarine, Coastal and Shelf Science,65, 239-252.
Gorokhova, E., Lehtiniemi, M., Postel, L., Rubene, G., Amid, C.,
Lesutiene, J., Uusitalo, L., Strake, S. & Demereckiene, N. (2016)
Indicator Properties of Baltic Zooplankton for Classification of
Environmental Status within Marine Strategy Framework Directive.Plos One, 11, e0158326.
Griffiths, J.R., Kadin, M., Nascimento, F.J., Tamelander, T., Törnroos,
A., Bonaglia, S., Bonsdorff, E., Brüchert, V., Gårdmark, A. &
Järnström, M. (2017) The importance of benthic–pelagic coupling for
marine ecosystem functioning in a changing world. Global Change
Biology, 23, 2179-2196.
Gröhsler, T., Oeberst, R., Schaber, M., Larson, N. & Kornilovs, G.
(2013) Discrimination of western Baltic spring-spawning and central
Baltic herring (Clupea harengus L.) based on growth vs. natural tag
information. Ices Journal of Marine Science, 70,1108-1117.
Hansson, S., Hobbie, J.E., Elmgren, R., Larsson, U., Fry, B. &
Johansson, S. (1997) The stable nitrogen isotope ratio as a marker of
food‐web interactions and fish migration. Ecology, 78,2249-2257.
Hislop, J., Bromley, P., Daan, N., Gislason, H., Heessen, H., Robb, A.,
Skagen, D., Sparholt, H. & Temming, A. (1997) Database report of the
stomach sampling project, 1991.
Hyslop, E. (1980) Stomach contents analysis—a review of methods and
their application. Journal of Fish Biology, 17, 411-429.
Jørgensen, H.B., Hansen, M.M., Bekkevold, D., Ruzzante, D.E. &
Loeschcke, V. (2005) Marine landscapes and population genetic structure
of herring (Clupea harengus L.) in the Baltic Sea.Molecular Ecology, 14, 3219-3234.
Kleppel, G. (1993) On the diets of calanoid copepods. Marine
Ecology-Progress Series, 99, 183-183.
Kulke, R. (2018) Investigations on the feeding behaviour of juvenile
sprat (Sprattus sprattus L.) and herring (Clupea harengusL.).
Larsen, T., Pollierer, M.M., Holmstrup, M., D’Annibale, A., Maraldo, K.,
Andersen, N. & Eriksen, J. (2016a) Substantial nutritional contribution
of bacterial amino acids to earthworms and enchytraeids: A case study
from organic grasslands. Soil Biology and Biochemistry,99, 21-27.
Larsen, T., Taylor, D.L., Leigh, M.B. & O’Brien, D.M. (2009) Stable
isotope fingerprinting: a novel method for identifying plant, fungal or
bacterial origins of amino acids. Ecology, 90,3526-3535.
Larsen, T., Ventura, M., Andersen, N., O’Brien, D.M., Piatkowski, U. &
McCarthy, M.D. (2013) Tracing Carbon Sources through Aquatic and
Terrestrial Food Webs Using Amino Acid Stable Isotope Fingerprinting.Plos One, 8, e73441.
Larsen, T., Ventura, M., Maraldo, K., Triadó‐Margarit, X., Casamayor,
E.O., Wang, Y.V., Andersen, N. & O’Brien, D.M. (2016b) The dominant
detritus‐feeding invertebrate in Arctic peat soils derives its essential
amino acids from gut symbionts. Journal of Animal Ecology .
Lartigue, J. & Cebrian, J. (2012) Ecosystem productivity and carbon
flows: patterns across ecosystems. The Princeton guide to ecology,
III, 9, 320-329.
Last, J. (1989) The food of herring, Clupea harengus , in the
North Sea, 1983–1986. Journal of Fish Biology, 34,489-501.
Marina, T.I., Saravia, L.A., Cordone, G., Salinas, V., Doyle, S.R. &
Momo, F.R. (2018) Architecture of marine food webs: To be or not be a
‘small-world’. Plos One, 13, e0198217.
McClelland, J.W. & Montoya, J.P. (2002) Trophic relationships and the
nitrogen isotopic composition of amino acids in plankton.Ecology, 83, 2173-2180.
McMahon, K.W., Berumen, M.L. & Thorrold, S.R. (2012) Linking habitat
mosaics and connectivity in a coral reef seascape. 109,15372-15376.
McMahon, K.W., Fogel, M.L., Elsdon, T.S. & Thorrold, S.R. (2010) Carbon
isotope fractionation of amino acids in fish muscle reflects
biosynthesis and isotopic routing from dietary protein. Journal of
Animal Ecology, 79, 1132-1141.
Möllmann, C., Diekmann, R., Müller-Karulis, B., Kornilovs, G., Plikshs,
M. & Axe, P. (2009) Reorganization of a large marine ecosystem due to
atmospheric and anthropogenic pressure: a discontinuous regime shift in
the Central Baltic Sea. Global Change Biology, 15,1377-1393.
Naumann, M., Umlauf, L., Mohrholz, V., Kuss, J., Siegel, H., Waniek, J.
& Schulz-Bull, D. (2017) Hydrographic-hydrochemical assessment of the
Baltic Sea 2016. Marine Science Reports . Meereswiss. Ber.,
Warnemünde.
O’Brien, D.M., Fogel, M.L. & Boggs, C.L. (2002) Renewable and
nonrenewable resources: Amino acid turnover and allocation to
reproduction in lepidoptera. Proceedings of the National Academy
of Sciences of the United States of America, 99, 4413-4418.
Ojaveer, H., Jaanus, A., MacKenzie, B.R., Martin, G., Olenin, S.,
Radziejewska, T., Telesh, I., Zettler, M.L. & Zaiko, A. (2010) Status
of biodiversity in the Baltic Sea. Plos One, 5, e12467.
Ojaveer, H., Lankov, A., Raid, T., Põllumäe, A. & Klais, R. (2018)
Selecting for three copepods - feeding of sprat and herring in the
Baltic Sea. Ices Journal of Marine Science, 75,2439-2449.
Ojaveer, H., Olenin, S., Narščius, A., Florin, A.-B., Ezhova, E.,
Gollasch, S., Jensen, K.R., Lehtiniemi, M., Minchin, D. &
Normant-Saremba, M. (2017) Dynamics of biological invasions and pathways
over time: a case study of a temperate coastal sea. Biological
Invasions, 19, 799-813.
Pejler, B. (1983) Zooplanktic indicators of trophy and their food.Forest water ecosystems , pp. 111-114. Springer.
Post, D.M. (2002) Using stable isotopes to estimate trophic position:
Models, methods, and assumptions. Ecology, 83, 703-718.
Post, D.M., Layman, C.A., Arrington, D.A., Takimoto, G., Quattrochi, J.
& Montaña, C.G. (2007) Getting to the fat of the matter: models,
methods and assumptions for dealing with lipids in stable isotope
analyses. Oecologia, 152, 179-189.
Qiu, D., Huang, L. & Lin, S. (2016) Cryptophyte farming by symbiotic
ciliate host detected in situ. Proceedings of the National Academy
of Sciences, 113, 12208-12213.
R-Development-Core-Team (2018) R: A language and environment for
statistical computing. R Foundation for Statistical Computing, Vienna,
Austria.
Reusch, T.B.H., Dierking, J., Andersson, H.C., Bonsdorff, E.,
Carstensen, J., Casini, M., Czajkowski, M., Hasler, B., Hinsby, K.,
Hyytiäinen, K., Johannesson, K., Jomaa, S., Jormalainen, V., Kuosa, H.,
Kurland, S., Laikre, L., MacKenzie, B.R., Margonski, P., Melzner, F.,
Oesterwind, D., Ojaveer, H., Refsgaard, J.C., Sandström, A., Schwarz,
G., Tonderski, K., Winder, M. & Zandersen, M. (2018) The Baltic Sea as
a time machine for the future coastal ocean. Science Advances,4 .
Rowe, A.G., Iken, K., Blanchard, A.L., O’Brien, D.M., Døving Osvik, R.,
Uradnikova, M. & Wooller, M.J. (2019) Sources of primary production to
Arctic bivalves identified using amino acid stable carbon isotope
fingerprinting. Isotopes in Environmental and Health
Studies , 1-19.
Šaškov, A., Šiaulys, A., Bučas, M. & Daunys, D. (2014) Baltic herring
(Clupea harengus membras) spawning grounds on the Lithuanian coast:
current status and shaping factors**This study was supported by the
Norwegian Financial Mechanism (project No. LT0047). Oceanologia,56, 789-804.
Scott, J.H., O’Brien, D.M., Emerson, D., Sun, H., McDonald, G.D.,
Salgado, A. & Fogel, M.L. (2006) An examination of the carbon isotope
effects associated with amino acid biosynthesis. Astrobiology,6, 867-880.
Sommer, U., Meusel, B. & Stielau, C. (1999) An experimental analysis of
the importance of body-size in the seastar-mussel predator-prey
relationship. Acta Oecologica, 20, 81-86.
Soto, D.X., Wassenaar, L.I. & Hobson, K.A. (2013) Stable hydrogen and
oxygen isotopes in aquatic food webs are tracers of diet and provenance.Functional Ecology, 27, 535-543.
St. John Glew, K., Graham, L.J., McGill, R.A.R. & Trueman, C.N. Spatial
models of carbon, nitrogen and sulphur stable isotope distributions
(isoscapes) across a shelf sea: An INLA approach. Methods in
Ecology and Evolution, 0 .
Svensson, E., Schouten, S., Hopmans, E.C., Middelburg, J.J. & Damste,
J.S.S. (2016) Factors controlling the stable nitrogen isotopic
composition (δ15N) of lipids in marine animals.PLoS ONE, 11 .
Torniainen, J., Lensu, A., Vuorinen, P.J., Sonninen, E., Keinänen, M.,
Jones, R.I., Patterson, W.P. & Kiljunen, M. (2017) Oxygen and carbon
isoscapes for the Baltic Sea: Testing their applicability in fish
migration studies. Ecology and Evolution, 7, 2255-2267.
Vane, K., Larsen, T., Scholz-Böttcher, B.M., Kopke, B. & Ekau, W.
(2018) Ontogenetic resource utilization and migration reconstruction
with δ13C values of essential amino acids in theCynoscion acoupa otolith. Ecology and Evolution,8, 9859-9869.
Vokhshoori, N., Larsen, T. & McCarthy, M. (2014) Reconstructing
δ13C isoscapes of phytoplankton production in a
coastal upwelling system with amino acid isotope values of littoral
mussels. Marine Ecology Progress Series, 504, 59-72.
Wasmund, N., Dutz, J., Pollehne, F., Siegel, H. & Zettler, M.L. (2017)
Biological assessment of the Baltic Sea 2016. Marine Science
Reports . Meereswiss. Ber., Warnemünde.
Whiteman, J.P., Elliott Smith, E.A., Besser, A.C. & Newsome, S.D.
(2019) A Guide to Using Compound-Specific Stable Isotope Analysis to
Study the Fates of Molecules in Organisms and Ecosystems.Diversity, 11, 8.
Woodward, G., Speirs, D.C., Hildrew, A.G. & Hal, C. (2005)
Quantification and resolution of a complex, size-structured food web.Advances in Ecological Research, 36, 85-135.
Table 1. Sampling summary for research cruise AL476 with research vessel
ALKOR in April 2016. CSIA indicates the number of specimens analysed for
compound specific stable isotope analysis and BSIA the number of
specimens analysed for bulk stable isotope analysis.