Abstract
The fatty acid (FA) composition of spionids co-occurring in shallow water and occupying various habitats was analyzed to characterize spectrum and diversity of their food sources and elucidate their feeding habits and trophic relationships. These included free-living and tube-dwelling species, and also opportunistic and specialized shell-borers and their hosts. A plot of principal component analysis (PCA) scores based on the FA compositions of nine spionid species recognized five distinct groups with different feeding strategies and revealed differences not only between the species, but also within the same species from various habitats. The predominance of 20:5n-3, C16 polyunsaturated FAs, and 16:1n-7 in suspension feeders indicated that they feed on diatoms. Benthic dinoflagellates and diatoms, as well as bacteria, constituted a major part in the diet of deposit feeders. On the basis of high 22:6n-3 and 18:1n-9 contents, Dipolydora commensalis was attributed to omnivorous with a predominance of animal dietary input. The selective detritivore Polydora glycymerica relies on a microbial food web. FAs of Laonice aff. cirrata indicated the importance of foraminifera in the diet of this subsurface feeder. Polychaetes were found to have a capability of changing their feeding habits depending on habitat. Specialized shell-borers adapt their feeding habits to the host’s diet. The results obtained provide evidence that these species actually represent several non-overlap** groups characterized by different feeding strategies, which leads to weakening of their competitive relationships. Partitioning of food sources is regarded as one of the main mechanisms explaining the successful coexistence of spionid species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated and analyzed during this study are included in this published article.
References
Andresen M, Kristensen E (2002) The importance of bacteria and microalgae in the diet of the deposit-feeding polychaete Arenicola marina. Ophelia 56:179–196. https://doi.org/10.1080/00785236.2002.10409498
Baiser B, Ardeshiri RS, Ellison AM (2011) Species richness and trophic diversity increase decomposition in a co-evolved food web. PLoS ONE 6(5):e20672. https://doi.org/10.1371/journal.pone.0020672
Becker C, Türkay M (2017) Host specificity and feeding in European pea crabs (Brachyura, Pinnotheridae). Crustaceana 90:819–844. https://doi.org/10.1163/9789004366435_006
Blake JA (1996) Family Spionidae Grube 1850. In: Blake JA, Hilbig B, Scott PH (eds) The Annelida: Part 3 Polychaeta: Orbiniidae to Cossuridae. Santa Barbara Museum of Natural History, Santa Barbara California, pp 81–224
Blake JA, Maciolek NJ, Meißner K (2020) Spionidae Grube. In: Purschke G, Böggemann M, Westheide W (eds) Handbook of zoology: annelida Volume 2: Pleistoannelida, Sedentaria II. De Gruyter, Berlin, pp 1–103
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917. https://doi.org/10.1139/o59-099
Braeckman U, Provoost P, Sabbe K, Soetaert K, Middelburg JJ, Vincx M, Vanaverbeke J (2012) Temporal dynamics in the diet of two marine polychaetes as inferred from fatty acid biomarkers. J Sea Res 68:6–19. https://doi.org/10.1016/j.seares.2011.11.003
Carreau JP, Dubacq JP (1978) Adaptation of macro-scale method to the micro-scale for fatty acid methyl transesterification of biological lipid extracts. J Chromatogr 151:384–390. https://doi.org/10.1016/S0021-9673(00)88356-9
Checon HH, Pardo EV, Amaral ACZ (2017) Breadth and composition of polychaete diets and the importance of diatoms to species and trophic guilds. Helgol Mar Res 70:19. https://doi.org/10.1186/s10152-016-0469-4
Christianen MJA, Middelburg JJ, Holthuijsen SJ, Jouta J, Compton TJ et al (2017) Benthic primary producers are key to sustain the Wadden Sea food web: stable carbon isotope analysis at landscape scale. Ecology 98:1498–1512. https://doi.org/10.1002/ecy.1837
Christie WW (2021) Methyl esters of FA. Archive of mass spectra. The lipid web. Available at https://www.lipidhome.co.uk/ms/methesters/me-arch/index.htm (accessed on 22 June 2021).
Daggers TD, Van Oevelen D, Herman PMJ, Boschker HTS, Van der Wal D (2020) Spatial variability in macrofaunal diet composition and grazing pressure on microphytobenthos in intertidal areas. Limnol Oceanogr 65:2819–2834. https://doi.org/10.1002/lno.11554
Dauer DM (1991) Functional morphology and feeding behavior of Polydora commensalis (Polychaeta: Spionidae). Ophelia Suppl 5:607–614
Dauer DM, Maybury CA, Ewing RM (1981) Feeding behavior and general ecology of several spionid polychaetes from the Chesapeake Bay. J Exp Mar Biol Ecol 54:21–38. https://doi.org/10.1016/0022-0981(81)90100-3
Dikaeva DR (2022) Polychaeta fauna in the northeastern Barents Sea. Vestnik of MSTU 25:79–90. https://doi.org/10.21443/1560-9278-2022-25-2-79-90
Drazen JC, Phleger CF, Guest MA, Nichols PD (2008) Lipid, sterols and fatty acids of abyssal polychaetes, crustaceans, and a cnidarian from the northeast Pacific Ocean: food web implications. Mar Ecol Prog Ser 372:157–167. https://doi.org/10.3354/meps07707
Dubois S, Laurent B, Cognie B, Beninger PG (2005) Particle capture and processing mechanism in Sabellaria alveolata (Polychaeta: Sabellariidae). Mar Ecol Prog Ser 301:159–171. https://doi.org/10.3354/meps301159
Fauchald K, Jumars PA (1979) The diet of worms: a study of polychaete feeding guilds. Oceanogr Mar Biol Annu Rev 17:193–284
Garneau M-È, Vincent WF, Terrado R, Lovejoy C (2009) Importance of particle-associated bacterial heterotrophy in a coastal Arctic ecosystem. J Mar Syst 75:185–197. https://doi.org/10.1016/j.jmarsys.2008.09.002
Graeve M, Kattner G, Piepenburg D (1997) Lipids in Arctic benthos: does the fatty acid and alcohol composition reflect feeding and trophic interactions? Polar Biol 18:53–61. https://doi.org/10.1007/s003000050158
Ha SY, Min WK, Kim DS, Shin KH (2014) Trophic importance of meiofauna to polychaetes in a seagrass (Zostera marina) bed as traced by stable isotopes. J Mar Biol Assoc UK 94:121–127. https://doi.org/10.1017/S0025315413001148
Hardin G (1960) The competitive exclusion principle. Science 131(3409):1292–1297. https://doi.org/10.1126/science.131.3409.1292
Haynert K, Gluderer F, Pollierer MM, Scheu S, Wehrmann A (2020) Food spectrum and habitat-specific diets of benthic foraminifera from the Wadden Sea – a fatty acid biomarker approach. Front Mar Sci 7:510288. https://doi.org/10.3389/fmars.2020.510288
Hentschel BT (2004) Sediment resuspension and boundary layer flow dramatically increase the growth rates of interface-feeding spionid polychaetes. J Mar Syst 49:209–224. https://doi.org/10.1016/j.jmarsys.2003.08.007
Hope JA, Paterson DM, Thrush SF (2019) The role of microphytobenthos in soft-sediment ecological networks and their contribution to the delivery of multiple ecosystem services. J Ecol 108:815–830. https://doi.org/10.1111/1365-2745.13322
Howell KL, Pond DW, Billett DSM, Tyler PA (2003) Feeding ecology of deep-sea seastars (Echinodermata: Asteroidea): a fatty acid biomarker approach Mar Ecol Prog Ser 255:193–206. https://doi.org/10.3354/meps266103
Jumars PA, Self RFL, Nowell ARM (1982) Mechanics of particle selection by tentaculate deposit-feeders. J Exp Mar Biol Ecol 64:47–70. https://doi.org/10.1016/0022-0981(82)90067-3
Jumars PA, Dorgan KM, Lindsay SM (2015) Diet of worms emended: an update of polychaete feeding guilds. Annu Rev Mar Sci 7:497–520. https://doi.org/10.1146/annurev-marine-010814-020007
Kaneda T (1991) Iso-and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol Rev 55:288–302 (PMID: 1886522)
Kang C-K, Kim JB, Lee K-S, Kim JB, Lee P-Y et al (2003) Trophic importance of benthic microalgae to macrozoobenthos in coastal bay systems in Korea: dual stable C and N isotope analyses. Mar Ecol Prog Ser 259:79–92. https://doi.org/10.3354/meps259079
Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar Ecol Prog Ser 446:1–22. https://doi.org/10.3354/meps09559
Kharlamenko VI, Zhukova NV, Khotimchenko SV, Svetashev VI, Kamenev GM (1995) Fatty-acids as markers of food sources in a shallow-water hydrothermal ecosystem (Kraternaya Bight, Yankich Island, Kurile Islands). Mar Ecol Prog Ser 120:231–241. https://doi.org/10.3354/meps120231
Klein Breteler WCM, Schogt N, Baas M, Schouten S, Kraay GW (1999) Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids. Mar Biol 135:191–198. https://doi.org/10.1007/s002270050616
Klootwijk AT, Sweetman AK, Hess S, Alve E, Dunlop KM, Renaud PE (2021) Benthic foraminiferal carbon cycling in coastal zone sediments: The influence of the assemblage structure and jellyfish detritus. Estuar Coast Shelf Sci 261:107535. https://doi.org/10.1016/j.ecss.2021.107535
Laureillard J, Mejanelle L, Sibuet M (2004) Use of lipids to study the trophic ecology of deepsea Xenophyophores. Mar Ecol Prog Ser 270:129–140. https://doi.org/10.3354/meps270129
Legeżyńska J, Kedra M, Walkusz W (2014) Identifying trophic relatioships within benthic community: how much can fatty acids tell? Mar Biol 161:821–836. https://doi.org/10.1007/s00227-013-2380-8
LeKieffre C, Spangenberg JE, Mabilleau G, Escrig S, Meibom A, Geslin E (2017) Surviving anoxia in marine sediments: The metabolic response of ubiquitous benthic foraminifera (Ammonia tepida). PLoS ONE 12(5):e0177604. https://doi.org/10.1371/journal.pone.0177604
Leroy F, Meziane T, Riera P, Comtet T (2013) Seasonal variations in maternal provisioning of Crepidula fornicata (Gastropoda): fatty acid composition of females, embryos and larvae. PLoS ONE 8(9):e75316. https://doi.org/10.1371/journal.pone.0075316
Mansour MP, Volkman JK, Jackson AE, Blackburn SI (1999) The fatty acid and sterol composition of five marine dinoflagellates. J Phycol 35:710–720. https://doi.org/10.1046/j.1529-8817.1999.3540710.x
Martin D, Britayev TA (1998) Symbiotic polychaetea: Review of known species. Oceanogr Mar Biol Annu Rev 36:217–340
Martin D, Britayev TA (2018) Symbiotic polychaetes revisited: an update of the known species and relationships (1998–2017). Oceanogr Mar Biol Annu Rev 56:371–448
Mayzaud P, Boutoute M, Noyon M et al (2013) Lipid and fatty acids in naturally occurring particulate matter during spring and summer in a high arctic fjord (Kongsfjorden, Svalbard). Mar Biol 160:383–398. https://doi.org/10.1007/s00227-012-2095-2
Nomaki H, Ogawa NO, Ohkouchi N, Suga H, Toyofuku T, Shimanaga M, Nakatsuka T, Kitazato H (2008) Benthic foraminifera as trophic links between phytodetritus and benthic metazoans: carbon and nitrogen isotopic evidence. Mar Ecol Prog Ser 357:153–164. https://doi.org/10.3354/meps07309
Nyssen F, Brey T, Dauby P, Graeve M (2005) Trophic position of Antarctic amphipods enhanced analysis by a 2-dimensional biomarker assay. Mar Ecol Prog Ser 300:135–145. https://doi.org/10.3354/meps300135
Oxtoby LE, Budge SM, Iken K, O’Brien DM, Wooller MJ (2016) Feeding ecologies of key bivalve and polychaete species in the Bering Sea as elucidated by fatty acid and compound-specific stable isotope analyses. Mar Ecol Prog Ser 557:161–175. https://doi.org/10.3354/meps11863
Perry GJ, Volkman JK, Johns RB, Bavor HJ (1979) Fatty acids of bacterial origin in contemporary marine sediments. Geochim Cosmochim Acta 43:1715–1725. https://doi.org/10.1016/0016-7037(79)90020-6
Phleger CF, Nelson MM, Groce AK, Craig Cary S, Coyne K, Gibson JAE et al (2005) Lipid biomarkers of deep-sea hydrothermal vent polychaetes Alvinella pompejana, A. caudata, Paralvinella grasslei and Hesiolyra bergii. Deep Sea Res Part I 52:2333–2352. https://doi.org/10.3354/meps07309
Plyuscheva M, Martin D, Britayev TA (2010) Diet analyses of the scale-worms Lepidonotus squamatus and Harmothoe imbricata (Polychaeta, Polynoidae) in the White Sea. Mar Biol Res 6:271–281. https://doi.org/10.1080/17451000903334694
Pond DW, Allen CE, Bell MV, Van Dover CL, Fallick AE, Dixon DR, Sargent JR (2002) Origins of long-chain polyunsaturated fatty acids in the hydrothermal vent worms Ridgea piscesae and Protis hydrothermica. Mar Ecol Prog Ser 225:219–226. https://doi.org/10.1007/BF00349690
Qian P-Y, Chia F-S (1997) Structure of feeding palps and feeding behavior of the spionid polychaete Polydora polybranchia. Bulletin Mar Sci 60:502–511
Radashevsky VI (1993) Revision of the genus Polydora and related genera from the North West Pacific (Polychaeta: Spionidae). Pub Seto Mar Biol Lab 36:1–60. https://doi.org/10.5134/176224
Riera P, Stal LJ, Nieuwenhuize J (2000) Heavy δ15N in intertidal benthic algae and invertebrates in the Scheldt Estuary (The Netherlands): effect of riverine nitrogen inputs. Estuar Coast Shelf Sci 51:365–372. https://doi.org/10.1006/ecss.2000.0684
Rouse GW, Pleijel F, Tilic E (2022) Polychaetes. Oxford University Press, New York, pp 1–432
Salvo F, Dufour SC, Hamoutene D, Parrish CC (2015) Lipid classes and fatty acids in Ophryotrocha cyclops, a Dorvilleid from Newfoundland aquaculture sites. PLoS ONE 10(8):e0136772. https://doi.org/10.1371/journal.pone.0136772
Sato-Okoshi W (1999) Polydorid species (Polychaeta: Spionidae) in Japan, with descriptions of morphology, ecology and burrow structure. 1. Boring species. J Mar Biol Assoc UK 79:831–848. https://doi.org/10.1017/S0025315498001003
Schenk S, Hoeger U (2010) Lipid accumulation and metabolism in polychaete spermatogenesis: Role of the large discoidal lipoprotein. Mol Reprod Dev 77:710–719. https://doi.org/10.1002/mrd.21208
Selina MS (2016) Seasonal and long-term dynamics of sand-dwelling dinoflagellates (Dinoflagellata) in Peter the Great Bay, Sea of Japan. Russ J Mar Biol 42:458–470. https://doi.org/10.1134/S1063074016060109
Silina AV, Zhukova NV (2009) Topical and trophic relationships in a boring polychaete–scallop association: fatty acid biomarker approach. Mar Ecol Prog Ser 394:125–136. https://doi.org/10.3354/meps08189
Southward EC (1957) The distribution of Polychaeta in offshore deposits in the Irish Sea. J Mar Biol Ass UK 36:49–75. https://doi.org/10.1017/s0025315400017069
Suhr SB, Pond DW, Gooday AJ, Smith CR (2003) Selective feeding by benthic foraminifera on phytodetritus on the western Antarctic Peninsula shelf: evidence from fatty acid biomarker analysis. Mar Ecol Prog Ser 262:153–162. https://doi.org/10.3354/meps262153
Taghon GL, Nowell ARM, Jumars PA (1980) Induction of suspension feeding in spionid polychaetes by high particulate fluxes. Science 210:562–564. https://doi.org/10.1126/science.210.4469.562
Taghon GL, Prahl FG, Sparrow M, Fuller CM (1994) Lipid class and glycogen content of the lugworm Abarenicola pacifica in relation to age, growth rate and reproductive condition. Mar Biol 120:287–329. https://doi.org/10.7282/T3P272BZ
Turney S, Buddle CM (2016) Pyramids of species richness: the determinants and distribution of species diversity across trophic levels. Oikos 125:1224–1232. https://doi.org/10.1111/oik.03404
van der Heijden LH, Graeve M, Asmus R, Rzeznik-Orignac J, Niquil N et al (2019) Trophic importance of microphytobenthos and bacteria to meiofauna in soft-bottom intertidal habitats: A combined trophic marker approach. Mar Environ Res 149:50–66. https://doi.org/10.1016/j.marenvres.2019.05.014
Volkman JK, Jeffrey SW, Nichols PD, Rogers GI, Garland CD (1989) Fatty acid and lipid composition of 10 species of microalgae used in mariculture. J Exp Mar Biol Ecol 128:219–240. https://doi.org/10.1016/0022-0981(89)90029-4
Williams JD (2006) The ecology and feeding biology of two Polydora species (Polychaeta: Spionidae) found to ingest the embryos of host hermit crabs (Anomura: Decapoda) from the Philippines. J Zool 257:339–351. https://doi.org/10.1017/S0952836902000948
Williams JD, McDermott JJ (1997) Feeding behavior of Dipolydora commensalis (Polychaeta: Spionidae): particle capture, transport, and selection. Invertebr Biol 116:115–123. https://doi.org/10.2307/3226975
Williams JD, McDermott JJ (2004) Hermit crab biocoenoses: A worldwide review of the diversity and natural history of hermit crab associates. J Expt Mar Biol Ecol 305:1–128. https://doi.org/10.1016/j.jembe.2004.02.020
Würzberg L, Peters J, Schuller M, Brandt A (2011) Diet insights of deepsea polychaetes derived from fatty acid analyses. Deep Sea Res Part II 58:153–162. https://doi.org/10.1016/j.dsr2.2010.10.014
Zhukova NV (1991) The pathway of the biosynthesis of non-methylene-interrupted dienoic fatty acids in mollusks. Comp Biochem Physiol B 100:801–804. https://doi.org/10.1016/0305-0491(91)90293-M
Zhukova NV, Aizdaicher NA (1995) Fatty acid composition of 15 species of marine microalgae. Phytochemistry 39:351–356. https://doi.org/10.1016/0031-9422(94)00913-E
Zhukova NV, Kharlamenko VI (1999) Sources of essential fatty acids in the marine microbial loop. Aquat Microb Ecol 17:153–157. https://doi.org/10.3354/ame017153
Zhukova NV, Eliseikina MG, Balakirev ES, Ayala FJ (2022) Multiple bacterial partners in symbiosis with the nudibranch mollusk Rostanga alisae. Sci Rep 12:169. https://doi.org/10.1038/s41598-021-03973-7
Acknowledgements
The author is grateful to Dr. Vasily I. Radashevsky for collection of animals, identification of the species, and for his critical comments on the earlier version of the manuscript. Special thanks goes to Evgeny Shvetsov for proofreading the English manuscript. The study was funded by the Federal Scientific and Technical Program in the field of environmental development of the Russian Federation and climate change for 2021 – 2030, Russian Federation (Project No 123080800009-5).
Funding
Federal Scientific and Technical Program in the field of environmental development of the Russian Federation and climate change, Russian Federation, Project No 123080800009-5.
Author information
Authors and Affiliations
Contributions
The study was conducted and written by NVZ.
Corresponding author
Ethics declarations
Conflict of interest
The author declares no competing interests.
Ethical approval
All applicable international and national guidelines for sampling and experimental use of organisms for the study have been followed and all necessary approvals have been obtained.
Additional information
Responsible Editor: N. Aberle-Malzahn.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhukova, N.V. Fatty acid analysis reveals variations in the diet of shallow-water spionids (Annelida: Polychaeta: Spionidae). Mar Biol 170, 162 (2023). https://doi.org/10.1007/s00227-023-04306-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-023-04306-0