Abstract
Irregular urchins exclusively live in marine soft bottom habitats, dwelling either upon or inside sediments and selectively picking up sediment grains and organic particles, or swallowing bulk sediment to feed on the associated organic matter. The exact food source and dietary requirements of most irregular echinoids, however, remain incompletely understood. The schizasterid species Abatus cordatus (Verrill, 1876) is a sub-Antarctic spatangoid that is endemic to the Kerguelen. The feeding behaviour of A. cordatus was investigated using simultaneously metabarcoding and stable isotope approaches. Comparison of ingested and surrounding sediments by metabarcoding revealed a limited selective ingestion of prokaryotes and eukaryotes by the urchin. Compared to surrounding sediments, the gut content had (i) higher carbon and nitrogen concentrations potentially due to selective ingestion of organic matter and/or the sea urchin mucus secretion and (ii) δ15N enrichment due to the selective assimilation of lighter isotope in the gut. Feeding experiments were performed using 13C and 15 N-enriched sediments in aquariums. The progression of stable isotope enrichment in proximal and distal parts of the digestive track of A. cordatus revealed that all particles are not similarly transported likely due to siphon functioning. Ingestion of water with associated dissolved and particulate organic matter should play an important role in urchin nutrition. A. cordatus had a gut resident time fluctuating between 76 and 101 h and an ingestion rate of 36 mg dry sediment h−1 suggesting that dense populations of the species may play a key ecological role through bioturbation in soft bottom shallow-water habitats of the Kerguelen Islands.
Similar content being viewed by others
References
Achatz JG, Chiodin M, Salvenmoser W, Tyler S, Martinez P (2013) The Acoela: on their kind and kinships, especially with nemertodermatids and xenoturbellids (Bilateria incertae sedis). Org Divers Evol 13:267–286
Allan EL, Froneman PW, Durgadoo JV, McQuaid CD, Ansorge IJ, Richoux NB (2013) Critical indirect effects of climate change on sub-Antarctic ecosystem functioning. Ecol Evol 3:2994–3004
Austen MC, Widdicombe S (1998) Experimental evidence of effects of the heart urchin Brissopsis lyrifera on associated subtidal meiobenthic nematode communities. J Exp Mar Biol Ecol 222:219–238
Bell SS, Coull BC (1978) Field evidence that shrimp predation regulates meiofauna. Oecologia 35:141–148
Bird FL, Ford PW, Hancock GJ (1999) Effect of burrowing macrobenthos on the flux of dissolved substances across the water-sediment interface. Mar Freshw Res 50:523–532
Blankenship LE, Yayanos AA (2005) Universal primers and PCR of gut contents to study marine invertebrate diets. Mol Ecol 14:891–899
Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotope in trophic ecology. Annu Rev Ecol Syst 42:411–440
Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Caporaso JG (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 17:90
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat biotechnol 37:852–857
Boon AR, Duineveld GCA (2012) Phytopigments and fatty acids in the gut of the deposit-feeding heart urchin Echinocardium cordatum in the southern North Sea: Selective feeding and its contribution to the benthic carbon budget. J Sea Res 67:77–84
Bromley RG, Asgaard U (1975) Sediment structures produced by a spatangoid echinoid: a problem of preservation. Bull Geol Soc Den 24:261–281
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP (2016) DADA2: High-resolution sample inference from illumina amplicon data. Nat Methods 13:581–583
Camprasse ECM, Cherel Y, Arnould JPY, Hoskins AJ, Bustamante P, Bost CA (2017a) Mate similarity in foraging Kerguelen shags: a combined bio-logging and stable isotope investigation. Mar Ecol Prog Ser 578:183–196
Camprasse ECM, Cherel Y, Bustamante P, Arnould JPY, Bost CA (2017b) Intra- and inter-individual variation in the foraging ecology of a generalist subantarctic seabird, the gentoo penguin. Mar Ecol Prog Ser 578:227–242
Cherel Y, Ducatez S, Fontaine C, Richard P, Guinet C (2008) Stable isotopes reveal the trophic position and mesopelagic fish diet of femal southern elephant seals breeding on the Kerguelen Islands. Mar Ecol Prog Ser 370:239–247
Collard M, De Ridder C, David B, Dehairs F, Dubois P (2014) Could the acid-base status of Antarctic sea urchins indicate a better than expected resiliens to near-future ocean acidification? Glob Change Biol 21:605–617
Criscuolo A, Brisse S (2013) AlienTrimmer: a tool to quickly and accurately trim off multiple short contaminant sequences from high-throughput sequencing reads. Genomics 102:500–506
De Ridder C (1987) Mécanique digestive chez l’echinide fouisseur Echinocardium cordatum (echinodermata). Bull Soc Sci Nat. 65–70
De Ridder C, Jangoux M (1985) Origine des sédiments ingérés et durée du transit digestif chez l’oursin spatangide, Echinocardium cordatum (Pennant) (Echinodermata). Ann Inst Oceanogr 61:51–58
De Ridder C, Jangoux M (1993) The digestive tract of the spatangoid echinoid Echinocardium cordatum (Echinodermata): morphofunctional study. Acta Zool 74:337–351
De Ridder C, Saucède T (2020) Echinocardium cordatum. In: Lawrence JM (ed) Sea urchins: biology and ecology, book 43. Elsevier, Amsterdam
De Ridder C, Jangoux M, Van Impe E (1985) Food selection and absorption efficiency in the spatangoid echinoid, Echinocardium cordatum (Echinodermata). In: Keegan B, O’Connor B (eds) Fifth International Echinoderm Conference. Balkema, Galway
De Ridder C, Jangoux M, de Vos L (1987) Frontal ambulacrum and peribuccal areas of the spatangoid echinoid Echinocardium cordatum(Echinodermata): a functional entity in feeding mechanism. Mar Biol 94:613–624
De Troch M, Boeckx P, Cnudde C, Van Gansbeke D, Vanreusel A, Vincx M, Caramujo M-J (2012) Bioconversion of fatty acids at the basis of marine food webs: insight from compound-specific stable isotope analysis. Mar Ecol Prog Ser 465:53–67
Dorgan KM, Jumars PA, Johnson BD, Boudreau BP (2006) Macrofaunal burrowing: the medium is the message. Ocean Mar Biol Ann Rev 44:85–121
Fabri-Ruiz S, Saucède T, Danis B, David B (2017) Southern ocean echinoids database. An updated version of Antarctic, Sub-Antarctic and cold temperate echinoid database. ZooKeys. https://doi.org/10.3897/zookeys.697.14746
Féral JP, Saucède T, Poulin E, Marschal C, Marty G, Roca JC, Motreuil S, Beurier JP (2016) PROTEKER: implementation of a submarine observatory at the Kerguelen Islands (Southern Ocean). Underw Technol 34:3–10
Fitzhugh GR, Fleeger JW (1985) Goby (Pisces: Gobiidae) interactions with meiofauna and small macrofauna. Bull Mar Sci 36:436–444
Fry B (1988) Food web structure on Georges Bank from stable C, N, and S isotopic compositions. Limnol Oceanogr 33:1182–1190
Fry B (2006) Stable isotope ecology. Springer, New-York
Fry B, Anderson RK, Entzeroth L, Bird JL, Parker PL (1984) 13C enrichment and oceanic food web structure in the Northwestern Gulf of Mexico. Contrib Mar Sci 27:49–63
Ghiold J (1989) Species distribution of irregular echinoids. Biol Oceanogr 6:79–162
Giere O (2009) Meiobenthology: the microscopic motile fauna of aquatic sediments. Springer, Berlin
Gilbert JM, Goldring R (2008) Spatangoid-produced ichnofabrics (Bateig Limestone, Miocene, Spain) and the preservationn of spatangoid trace fossils. Palaeogeogr Palaeoclimatol Palaeoecol 270:299–310
Grey J, Thackeray SJ, Jones RI, Shine A (2002) Ferox trout (Salmo trutta) as « Russian dolls »: complementary gut content and stable isotope analyses of the Loch Ness foodweb. Freshw Biol 47:1235–1243
Guelinckx J, Dehairs F, Ollevier F (2008) Effect of digestion on the δ13C and δ15N of fish-gut contents. J Fish Biol 72:301–309
Guillaumot C, Fabri-Ruiz S, Martin A, Eléaume M, Danis B, Féral JP, Saucède T (2018) Benthic species of the Kerguelen Plateau show contrasting distribution shifts in response to environmental changes. Ecol Evol 8:6210–6225
Gutt J, Bertler N, Bracegirdle TJ, Bushmann A, Comiso J, Hosie G, Isla E, Schloss IR, Smith CR, Tournadre J, Xavier JC (2015) The Southern Ocean ecosystem under multiple climate change stress: an integrated circumpolar assessment. Glob Change Biol 21:1434–1453
Hammond LS (1981) An analysis of grain size modification in biogenic carbonate sediments by deposit-feeding holothurians and echinoids (Echinodermata). Limnol Oceanogr 26:898–906
Hammond LS (1982a) Analysis of grain-size selection by deposit-feeding holothurians and echinoids (Echinodermata) from a shallow reef lagoon, Discovery Bay, Jamaica. Mar Ecol Prog Ser 8:25–36
Hammond LS (1982b) Patterns of feeding and activity in deposit-feeding holothurians and echinoids (echinodermata) from a shallow back-reef lagoon, Discovery Bay, Jamaica. Bull Mar Sci 32:549–571
Hammond LS (1983) Nutrition of deposit-feeding holothuroids and echinoids (Echinodermata) from a shallow reef lagoon, Discovery Bay, Jamaica. Mar Ecol Prog Ser 10:297–305
Henry BA, Jenkins GP (1995) The impact of predation by the girled goby, Nesogobius sp. 1, on abundances of meiofauna and small macrofauna. J Exp Mar Biol Ecol 191:223–238
Holland ND (2013) Digestive system. In: Lawrence JM (ed) Sea urchins: biology and ecology. Academic Press, San Diego
Holland ND, Ghiselin MT (1970) A comparative study of gut mucuous cells in thirty-seven species of the class Echinoidea (Echinodermata). Biol Bull (Woods Hole) 138:286–305
Hollertz K (2002) Feeding biology and carbon budget of the sediment-burrowing heart urchin Brissopsis lyrifera (Echinoidea: Spatangoida). Mar Biol 140:959–969
Hollertz K, Duchêne J-C (2001) Burrowing behaviour and sediment reworking in the heart urchin Brissopsis lyrifera Forbes (Spatangoida). Mar Biol 139:951–957
Jangoux M, Lawrence JM (1982) Echinoderm nutrition. Balkema Press, Rotterdam
Jennings JB (1971) Parasitism and commensalism in the Turbellaria. Adv Parasit 9:1–32
Johnson JS, Raubenheimer D, Bury SJ, Clements KD (2012) Effect of ingestion on the stable isotope signatures of marine herbivorous fish diets. J Exp Mar Biol Ecol 438:137–143
Jumars PA (1993) Gourmands of mud: diet selection in marine deposit feeders. In: Hughes RN (ed) Mechanisms of diets choice. Blackwell Scientific Publishers, Oxford
Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373:275–284
Kurihara H, Shiarayama Y (2004) Effects of increased atmospheric CO2 on sea urchin early development. Mar Ecol Prog Ser 274:161–169
Ledoux JB, Tarnowska K, Gérard K, Lhuiller E, Jacquemin B, Weydmann A, Féral JP, Chenuil A (2012) Fine-scale spatial genetic structure in the brooding sea urchin Abatus cordatus suggests vulnerability of the Southern Ocean marine invertebrates facing global change. Pol Biol 35:611–623
Leduc D, Probert PK, Duncan A (2009) A multi-method approach for identifying meiofaunal trophic connections. Mar Ecol Prog Ser 383:95–111
Lohrer AM, Thrush SF, Gibbs M (2004) Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431:1092–1095
Lopez GR, Levinton JS (1987) Ecology of deposit-feeding animals in marine sediments. Q Rev Biol 62:235–260
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550
McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390
Michel LN, David B, Dubois P, Lepoint G, De Ridder C (2016) Trophic plasticity of Antarctic echinoids under contrasted environmental conditions. Pol Biol 39:913–923
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chain: further evidence and the δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140
Mooi R (1990) Paedomorphosis, Aristotle’s lantern, and the origin of the sand dollar (Echinodermata: Clypeasteroida). Paleobiology 16:25–48
Nilsson P, Sundback K, Jonsson B (1993) Effect of the brown shrimp Crangon crangon on endobenthic macrofauna, meiofauna and meiofaunal grazing rates. Neth J Sea Res 31:95–106
Olive PJW, Pinnegar JK, Polunin NVC, Richards G, Welch R (2003) Isotope trophic-step fractionation: a dynamic equilibrium model. J Anim Ecol 72:608–617
Osinga R, Kop AJ, Malschaert JFP, van Duyl FC (1997) Effects of the sea urchin Echinocardium cordatum on bacterial production and carbon flow in experimental benthic systems under increasing organic loading. J Sea Res 37:109–121
Pascal PY, Dupuy C, Mallet C, Richard P, Niquil N (2008) Bacterivory by benthic organism in sediment: quantification using 15N-enriched bacteria. J Exp Mar Biol Ecol 355:18–26
Pascal PY, Bocher P, Lefrançois C, Nguyen TH, Chevalier J, Dupuy C (2019) Meiofauna versus macrofauna as food resource in a tropical intertidal mudflat. Mar Biol 166:144
Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B, Grisel O, Blondel M, Prettenhofer P, Weiss R, Dubourg V, Vanderplas J, Passos A, Cournapeau D, Brucher M, Perrot M, Duchesnay E (2011) Scikit-learn: machine learning in python. J Mach Learn Res 12:2825–28300
Peterson B, Fry B, Deegan LA, Hershey A (1993) The trophic significance of epilithic algal production in a fertilized tundra river ecosystem. Limnol Oceanogr 38:872–878
Plante C, Jumars PA, Baross JA (1990) Digestive associations between marine detritivores and bacteria. Annu Rev Ecol Syst 21:93–127
Poulin E, Féral JP (1995) Pattern of spatial distribution of a brood-protecting schizasterid echinoid, Abatus cordatus, endemic to the Kerguelen Islands. Mar Ecol Prog Ser 118:179–186
Poulin E, Féral JP (1997) Genetic structure of the brooding sea urchin Abatus cordatus, an endemic of the subantarctic Kerguelen Island. In: Mooi R, Telford M (eds) 9th Echinoderm conference. Balkema, San Fransisco
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
Quereda JJ, Dussurget O, Nahori MA, Ghozlane A, Volant S, Dillies MA, Regnault B, Kennedy S, Mondot S, Villoing B, Cossart P, Pizarro-Cerda J (2016) Bacteriocin from epidemic Listeria strains alters the host intestinal microbiota to favor infection. P Natl Acad Sci USA 113:5706–5711
Radwánski A, Wysocka A (2001) Mass aggregation of Middle Miocene spine-coated echinoids Echinocardium and their integrated eco-taphonomy. Acta Geol Pol 51:295–316
Rolet G, De Ridder C (2012) Transfer and incorporation of D-glucose across the wall of the gastric caecum, the stomach and the intestine of the echinoid Echinocardium cordatum. Cah Biol Mar 53:533–539
Rolet G, Ziegler A, De Ridder C (2012) Presence of a seawater-filled caecum in Echinocardium cordatum (Echinoidea: Spatangoida). J Mar Biol Ass UK 92:379–385
Saucède T, Guillaumot C, Michel L, Fabri-Ruiz S, Bazin A, Cabessut M, García-Berro A, Mateos A, Mathieu O, De Ridder C, Dubois P, Danis B, David B, Díaz C, Lepoint G, Motreuil S, Poulin E, Féral JP (2019) Modelling species response to climate change in sub-Antarctic islands: echinoids as a case study for the Kerguelen plateau. In: Welsford D, Dell J, Duhamel G (eds). The Kerguelen Plateau: marine ecosystem and fisheries. Australian Antarctic Division
Schatt P, Féral JP (1991) The brooding cycle of Abatus cordatus (Echinodermata: Spatangoida) at Kerguelen Islands. Pol Biol 11:283–292
Schratzberger M, Ingels J (2018) Meiofauna matters: the role of meiofauna in benthic ecosystems. J Exp Mar Biol Ecol 502:12–25
Schwob G, Cabrol L, Poulin E, Orlando J (2020) Characterization of the gut microbiota of the antarctic heart urchin (Spatangoida) Abatus agassizzi. Front Microbiol 11:308
Self RFL, Jumars PA (1978) New ressource axes for deposit feeders? J Mar Res 36:627–641
Steneck RS (2013) Sea urchins as drivers of shallow marine community structure. In: Lawrence JM (ed) Sea urchins: biology and ecology. Academic Press, San Diego
Thompson BAW, Riddle MJ (2005) Bioturbation behaviour of the spatangoid urchin Abatus ingens in Antarctic marine sediments. Mar Ecol Prog Ser 290:135–143
Thorsen MS (1998) Microbial activity, oxygen status and fermentation in the gut of the irregualr sea urchin Echinocardium cordatum (Spatangoida: echinodermata). Mar Biol 132:423–433
van Oevelen D, Middelburg JJ, Soetaert K, Moodley L (2006) The fate of bacterial carbon in sediments: modeling an in situ isotope tracer experiment. Limnol Oceanogr 51:1302–1314
Vopel K, Vopel A, Thistle D, Hancock N (2007) Effects of spatangoid heart urchins on O2 supply into coastal sediment. Mar Ecol Prog Ser 333:161–171
Weimerskirch H, Inchausti P, Guinet C, Barbraud C (2003) Trends in birds ans seals populations as indicators of a system shift in the Southern Ocean. Antarct Sci 15:249–256
Widdicombe S, Austen MC, Kendall MA, Warwick RM, Jones MB (2000) Bioturbation as a mechanism for setting and maintaining levels of diversity in subtidal macrobenthic communities. Hydrobiologia 440:369–377
Yatsuya K, Nakahara H (2004) Diet and stable isotope ratios of gut contents and gonad of the sea urchin Anthorcidaris crassispina (A. Agassiz) in two different adjacent habitats, the Sargassum area and Corallina area. Fish Sci 700:285–292
Acknowledgements
This study is a contribution to program PROTEKER (No. 1044) of the French Polar Institute and LTSER Zone ATelier Antarctique (ZATA, France). Work in the field also benefited from the support of the National Nature Reserve of the French Southern Territories and its staff and from Chilean PIA CONICYT ACT172065 for EP. We are particularly indebted to Gilles Marty, Sebastien Motreuil and to the crew of the boat Le Commerson for their invaluable help and support in the field. We would like to thank Stanislas Dubois for helpful comments about stable isotope data and Gérard Duineveld for useful suggestions. Metabarcoding sequencing performed at Biomics Platform, C2RT, Institut Pasteur, Paris, France, supported by France Génomique (ANR-10-INBS-09-09) and IBISA.
Author information
Authors and Affiliations
Contributions
PYP and TS conceived and design research. PYP, TS and EP realized the field work. PYP and TS conducted laboratory experiments. YR realized all the metabarcoding study. PYP wrote the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Authors have no conflict of interest to declare.
Additional information
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.
Supplementary file1 (PDF 348 KB)
Electronic Supplementary Material 1. Workflow implemented for eukaryotic metataxonomic analyses; ASV were extracted using QIIME2 pipeline; statistical analyses were performed using SHAMAN pipeline. Electronic Supplementary Material 2. Alpha diversity analysis based on alpha and Shannon indexes for sediments and Abatus cordatus samples; error bars represent 95% confidence intervals. Electronic Supplementary Material 3. Rarefaction curves of ASV for each sample.
Rights and permissions
About this article
Cite this article
Pascal, PY., Reynaud, Y., Poulin, E. et al. Feeding in spatangoids: the case of Abatus Cordatus in the Kerguelen Islands (Southern Ocean). Polar Biol 44, 795–808 (2021). https://doi.org/10.1007/s00300-021-02841-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-021-02841-4