Abstract
This study focuses on the analyses of the gastral cavity contents of two species of Ceriantharia, namely Isarachnanthus nocturnus Hartog, 1977, collected in São Sebastião, Brazil, and Pachycerianthus magnus Nakamoto, 1919, collected from two points along the coast of Okinawa Island, Japan. Both morphological (light microscopy) and metagenomic (whole-genome shotgun sequencing) analyses were conducted with the aim of identifying the main classes of organisms that make up the diet of these species. The results revealed that morphological analyses were not sufficient for identifying prey organisms, but metagenomic analyses showed a diverse range of animal classes, indicating the varied diet of these ceriantharians. The most abundant classes observed in the contents of both species were Anthozoa, Aconoidasida, Kinetoplastea, Actinopterygii, Insecta, and Leptocardii. This finding suggests a cohesive feeding pattern among these two species from distant areas, providing a more comprehensive understanding of their feeding performance and contributing to studies on the subclass Ceriantharia.
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References
Acuña FH, Zamponi MO (1995) Feeding ecology of intertidal sea anemones (Cnidaria, Actiniaria): food sources and trophic parameters. Biociências 3:73–84
Acuña FH, Zamponi MO (1996) Ecología trófica de las anémonas intermareales Phymactis clematis (Dana, 1849) Aulactinia marplatensis (Zamponi, 1977) y A. reynaudi (Milne-Edwards, 1857) (Actiniaria: Actiniidae): relaciones entre las anémonas y sus presas. Cienc Mar 22(4):397–413
Acuña FH, Excoffon AC, Genzano GN (2001) Feeding of Anthothoe chilensis (Actiniaria, Sagartiidae) in mar del Plata Port (Buenos Aires, Argentina). Biociências 9(1):111–120
Acuña FH, Excoffon AC, Zamponi MO, Genzano GN (2004) Feeding habits of the temperate octocoral Tripalea clavaria (Studer, 1878) (Octocorallia, Gorgonaria, Anthothelidae), from sublittoral outcrops off mar del Plata, Argentina. Belg J Zool 134(1):65–66
Blankenship LE, Yayanos AA (2005) Universal primers and PCR of gut contents to study marine invertebrate diets. Mol Ecol 14(3):891–899. https://doi.org/10.1111/j.1365-294x.2005.02448.x
Broderick NA, Lemaitre B (2012) Gut-associated microbes of Drosophila melanogaster. Gut Microbes 3(4):307–312. https://doi.org/10.4161/gmic.19896
Bursey CR, Guanciale JM (1977) Feeding behavior of the sea anemone Condylactis gigantea. Comp Biochem Physiol 57A:115–117
Celis JS, Wibberg D, Ramírez-Portilla C, Rupp O, Sczyrba A, Winkler A, Kalinowski J, Wilke T (2018) Binning enables efficient host genome reconstruction in Cnidarian Holobionts. GigaScience 7(7):1–12. https://doi.org/10.1093/gigascience/giy075
Ceriello H, Lopes CSS, Reimer JD, Bakken T, Fukuda MV, Cunha CM, Stampar SN (2020) Knock knock, who’s there?: marine invertebrates in tubes of Ceriantharia (Cnidaria: Anthozoa). Biodivers Data J 8:e47019. https://doi.org/10.3897/BDJ.8.e47019
Chintiroglou C, Koukouras A (1991) Observations on the feeding habits of Calliactis parasitica (Couch, 1842), Anthozoa Cnidaria. Oceanol Acta 14(4):389–396
Chintiroglou C, Koukouras A (1992) The feeding habits of three mediterranean sea anemone species, Anemonia viridis (Forskål), Actinia equina (Linnaeus) and Cereus pedunculatus (Pennant). Helgol Meeresunters 46(1):53–68. https://doi.org/10.1007/bf02366212
Conti-Jerpe IE, Thompson PD, Wong CWM, Oliveira NL, Duprey NN, Moynihan MA, Baker DM (2020) Trophic strategy and bleaching resistance in reef-building corals. Sci Adv 6(15):eaaz5443. https://doi.org/10.1126/sciadv.aaz5443
Davenport J, Moloney TV, Kelly J (2011) Common sea anemones Actinia equina are predominantly sessile intertidal scavengers. MEPS 430:147–155. https://doi.org/10.3354/meps08861
Eleftheriou A, Basford DJ (1983) The general behaviour and feeding of Cerianthus lloydIi, Gosse (Anthozoa, Coelenterata). Cah Biol Mar 24:147–158
Engelen AH, Aires T, Vermeij MJA, Herndl GJ, Serrão EA, Frade PR (2018) Host differentiation and compartmentalization of microbial communities in the Azooxanthellate Cupcorals Tubastrea coccinea and Rhizopsammia goesi in the Caribbean. Front Mar Sci 5:391. https://doi.org/10.3389/fmars.2018.00391
Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG, Sogin ML, Delmont TO (2015) Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ 3:e1319. https://doi.org/10.7717/peerj.1319
Ferrier-Pagès C, Witting J, Tambutté E, Sebens KP (2003) Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22(3):229–240. https://doi.org/10.1007/s00338-003-0312-7
Fraune S, Bosch TCG (2010) Why bacteria matter in animal development and evolution. BioEssays 32:571–580. https://doi.org/10.1002/bies.200900192
Gilbert JA, Dupont CL (2011) Microbial metagenomics: beyond the genome. Ann Rev Mar Sci 3:347–371. https://doi.org/10.1146/annurev-marine-120709-142811
Ivanova NY, Grebelnyi SD (2017) On the food of the Antarctic sea anemone Urticinopsis antarctica Carlgren, 1927 (Actiniidae, Actiniaria, Anthozoa). J Mar Biol Assoc 97(1):29–34. https://doi.org/10.1017/S0025315415002131
Jaenicke S, Albaum SP, Blumenkamp P, Linke B, Stoye J, Goesmann A (2018) Flexible metagenome analysis using the MGX framework. Microbiome 6(1):76. https://doi.org/10.1186/s40168-018-0460-1
Kuanui P, Chavanich S, Viyakarn V, Park HS & Omori M (2016) Feeding behaviors of three tropical scleractinian corals in captivity. Trop Zool 29(1):1-9. https://doi.org/10.1080/03946975.2015.1119006
Klompen AML, Macrander J, Reitzel AM, Stampar SN (2020) Transcriptomic analysis of four cerianthid (Cnidaria, Ceriantharia) venoms. Mar Drugs 18(8):413. https://doi.org/10.3390/md18080413
Lasker HR (1976) Intraspecific variability of zooplankton feeding in the hermatypic coral Montastrea cavernosa. In: Mackie GO (ed) Coelenterate ecology and behavior. Springer, New York, pp 101–109
Lasker HR (1981) A comparison of the particulate feeding abilities of three species of gorgonian soft coral. Mar Ecol Prog Ser 5(6):61-67
Leal MC, Rocha RJM, Anaya-Rojas JM, Cruz ICS, Ferrier-Pagès C (2017) Trophic and stoichiometric consequences of nutrification for the intertidal tropical zoanthid Zoanthus sociatus. Mar Pollut Bull 119(1):169–175. https://doi.org/10.1016/j.marpolbul.2017.03.054
Leibold MA (1995) The Niche concept revisited: mechanistic models and community context. Ecology 76:1371–1382
Leray M, Knowlton N (2015) DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. PNAS 112(7):2076–2081. https://doi.org/10.1073/pnas.1424997112
Leray M, Meyer CP, Mills SC (2015) Metabarcoding dietary analysis of coral dwelling predatory fish demonstrates the minor contribution of coral mutualists to their highly partitioned, generalist diet. PeerJ 3:e1047. https://doi.org/10.7717/peerj.1047
Menzel P, Ng KL, Krogh A (2016) Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun 7(1):1–9. https://doi.org/10.1038/ncomms11257
Nyholm KG (1943) Zur Entwicklung und Entwicklungsbiologie der Ceriantharien und Aktinien
Newsome SD, Martinez del Rio C, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5(8):429–436. https://doi.org/10.1890/060150.1
Olafsson EB, Peterson CH, Ambrose WGJ (1994) Does recruitment limitation structure populations and communities of macro-invertebrates in marine soft sediments: the relative significance of pre-and post-settlement processes. Oceanogr Mar Biol 32:65–109
Orejas C, Gili J, López-González PJ, Arntz W (2002) Feeding strategies and diet composition of four Antarctic Cnidarian species. Polar Biol 24(8):620–627. https://doi.org/10.1007/978-3-642-59419-9_19
Panikkar NK (1947) Observations on the structure and developmental stages of a new species of Arachnactis from the Madras plankton. Ann Sci Nat 9:227–250
Price WS, Lewis JJ (1975) Feeding mechanisms and feeding strategies of Atlantic reef corals. J Zool 176:527–544
Ribes M, Coma R, Gili JM (1999a) Seasonal variation of particulate organic carbon, dissolved organic carbon and the contribution of microbial communities to the live particulate organic carbon in a shallow near-bottom ecosystem at the Northwestern Mediterranean Sea. J Plankton Res 21(6):1077–1100
Ribes M, Coma R, Gili JM (1999b) Heterogeneous feeding in benthic suspension feeders: the natural diet and grazing rate of the temperate gorgonian Paramuricea clavata (Cnidaria: Octocorallia) over a year cycle. MEPS 183:125–137
Ribes M, Coma R, Rossi S (2003) Natural feeding of the temperate asymbiotic octocoral-gorgonian Leptogorgia sarmentosa (Cnidaria: Octocorallia). MEPS 254:141–150. https://doi.org/10.3354/meps254141
Stampar SN, Maronna MM, Vermeij MJA, Silveira FLd, Morandini AC (2012) Evolutionary diversification of banded tube-dwelling anemones (Cnidaria; Ceriantharia; Isarachnanthus) in the Atlantic Ocean. PLoS ONE 7(7):41091. https://doi.org/10.1371/journal.pone.0041091
Stampar SN, Morandini AC, Branco LC, Silveira FL, Migotto AE (2015) Drifting in the oceans: Isarachnanthus nocturnus (Cnidaria, Ceriantharia, Arachnactidae), an anthozoan with an extended planktonic stage. Mar Biol 162:2161–2169. https://doi.org/10.1007/s00227-015-2747-0
Stampar SN, Maronna MM, Kitahara MV, Reimer JD, Beneti JS, Morandini AC (2016) Ceriantharia in current systematics: life cycles, morphology and genetics. In: Goffredo S, Dubinsky Z (eds) The Cnidaria, Past, Present and Future. Springer, pp 61–72. https://doi.org/10.1007/978-3-319-31305-4_5
Stampar SN, Broe MB, Macrander J, Reitzel AM, Brugler MR, Daly M (2019) Linear mitochondrial genome in Anthozoa (Cnidaria): a case study in Ceriantharia. Sci Rep 9(1):6094. https://doi.org/10.1038/s41598-019-42621-z
Stampar SN, Reimer JD, Maronna MM, Lopes CSS, Ceriello H, Santos TB, Acuña FH, Morandini AC (2020) Ceriantharia (Cnidaria) of the World: an annotated catalogue and key to species. ZooKeys 952:1–63. https://doi.org/10.3897/zookeys.952.50617
Stampar SN (2012) Ceriantharia: a Retomada De Um Clado Esquecido. PhD Thesis, Instituto de Biociências da Universidade de São Paulo, Departamento de Zoologia
Symondson WOC (2002) Molecular identification of prey in predator diets. Mol Ecol 11(4):627–641. https://doi.org/10.1046/j.1365-294x.2002.01471.x
Tietjen M (2014) You are what you eat: how diet can influence the gut microbiota of marine invertebrates. Plymouth St Scient 7(2):203–211
Tsurpalo AP, Kostina EE (2003) Feeding characteristics of three species of intertidal Sea Anemones of the South Kuril Islands. Russ J Mar Biol 29(1):31–40. https://doi.org/10.1023/a:1022823819872
Zamer WE (1986) Physiological energetics of the intertidal sea anemone Anthopleura elegantissima. Mar Biol 92(3):299–314
Acknowledgements
This study was supported by São Paulo Research Foundation (FAPESP) [Proc. n. 2018/07622-0, 2019/14236-2, 2019/03552-0 and 2022/16193-1]. SNS was supported by National Council of Scientific and Technological Development (CNPq -Research Productivity Scholarship) grant number 301293/2019-8 and 304267/2022-8. We are grateful to all the MISE laboratory members for providing laboratory and technical support and to Dr. André C. Morandini (IB-USP) who provided constructive comments on the early version of the manuscript
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Santos, T.B., Poliseno, A., Bendia, A.G. et al. Unlocking the jar: revealing gastric content in Ceriantharia (Cnidaria, Anthozoa) through whole-genome shotgun sequencing. Aquat Ecol (2023). https://doi.org/10.1007/s10452-023-10076-0
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DOI: https://doi.org/10.1007/s10452-023-10076-0