Abstract
The speciose scarinine clade of coral reef parrotfishes display significant variation in trophic cranial morphology, yet are often described as generalist herbivores. The hypothesis that many parrotfishes target micro-photoautotrophs is a new framework within which to clarify parrotfish diets. Here, we investigate the dietary targets of Scarus rubroviolaceus using the feeding substrata extraction method and then compare the results to fourteen other syntopic parrotfish species. Scarus rubroviolaceus were followed on snorkel until repeated biting was observed. A 22 mm × 20 mm core was extracted around the bite. We identified and quantified the bite core biota by scraping the top 1 mm from bite cores for microscopy and 16S/18S small subunit rRNA metabarcoding. Filamentous cyanobacteria density on S. rubroviolaceus bite cores did not differ from the other fourteen parrotfish species, Calothrix (Nostocales) being the most frequently observed filamentous cyanobacteria for all fifteen parrotfish species. The 18S metabarcoding analysis detected the encrusting, endolithic sponge taxon Clionaida in the S. rubroviolaceus bite cores. We investigated the possibility of spongivory across all fifteen parrotfish species including an analysis of sponge-associated microbiota detected on the bite cores. This revealed a new axis of trophic partitioning with varying levels of spongivory amongst the fifteen Indo-Pacific parrotfish species. The bite cores of Cetoscarus ocellatus, Chlorurus spilurus, Chlorurus microrhinos, Scarus frenatus and S. rubroviolaceus particularly indicated spongivory. Our findings develop our understanding of parrotfish diet and provide further evidence that parrotfishes are specialized feeders and partition benthic trophic resources.
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The authors confirm that the data supporting the findings of this study are available within the article and its Supplementary material. Raw data are available from the corresponding author, upon reasonable request.
References
Acker K, Risk MJ (1985) Substrate destruction and sediment production by the boring sponge Cliona caribbaea on Grand Cayman Island. J Sediment Petrol 55:705–711
Alfaro ME, Brock CD, Banbury BL, Wainwright PC (2009) Does evolutionary innovation in pharyngeal jaws lead to rapid lineage diversification in labrid fishes? BMC Evol Biol 9:255. https://doi.org/10.1186/1471-2148-9-255
Arjunwadkar CV, Tebbett SB, Bellwood DR, Bourne DG, Smith HA (2022) Algal turf structure and composition vary with particulate loads on coral reefs. Mar Pollut Bull 181:113903. https://doi.org/10.1016/j.marpolbul.2022.113903
Bayer K, Jahn MT, Slaby BM, Moitinho-Silva L, Hentschel U (2018) Marine sponges as Chloroflexi hot spots: genomic insights and high-resolution visualization of an abundant and diverse symbiotic clade. mSystems. doi: https://doi.org/10.1128/mSystems.00150-18
Bellwood DR, Choat JH (1990) A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. Environ Biol Fishes 28:189–214. https://doi.org/10.1007/BF00751035
Bergquist P, Fromont P (1988) The marine fauna of New Zealand: Porifera, Demospongiae, Part 4 (Poecilosclerida). Wellington
Carballo JL, Bautista E, Nava H, Cruz-Barraza JA, Chávez JA (2013) Boring sponges, An increasing threat for coral reefs affected by bleaching events. Ecol Evol 3:872–886. https://doi.org/10.1002/ece3.452
Chanas B, Pawlik J (1995) Defenses of Caribbean sponges against predatory reef fish. II. Spicules, tissue toughness, and nutritional quality. Mar Ecol Prog Ser 127:195–211. https://doi.org/10.3354/meps127195
Choat JH, Klanten OS, Van Herwerden L, Robertson DR, Clements KD (2012) Patterns and processes in the evolutionary history of parrotfishes (Family Labridae). Biol J Lin Soc 107:529–557. https://doi.org/10.1111/j.1095-8312.2012.01959.x
Clements KD, Bellwood DR (1988) A comparison of the feeding mechanisms of two herbivorous labroid fishes, the temperate Odax pullus and the tropical Scarus rubroviolaceus. Mar Freshw Res 39:87. https://doi.org/10.1071/MF9880087
Clements KD, Choat JH (2018) Nutritional ecology of parrotfishes (Scarinae, Labridae). In: Hoey AS, Bonaldo RM (eds) Biology of parrotfishes. CRC Press, Boca Raton, FL, pp 42–68
Clements KD, German DP, Piché J, Tribollet A, Choat JH (2017) Integrating ecological roles and trophic diversification on coral reefs: multiple lines of evidence identify parrotfishes as microphages. Biol J Lin Soc 120:729–751. https://doi.org/10.1111/bij.12914
Coppock AG, Kingsford MJ, Battershill CN, Jones GP (2022) Significance of fish–sponge interactions in coral reef ecosystems. Coral Reefs 41:1285–1308. https://doi.org/10.1007/s00338-022-02253-8
Cowman PF, Bellwood DR (2011) Coral reefs as drivers of cladogenesis: expanding coral reefs, cryptic extinction events, and the development of biodiversity hotspots. J Evol Biol 24:2543–2562. https://doi.org/10.1111/j.1420-9101.2011.02391.x
de Bakker DM, Webb AE, van den Bogaart LA, van Heuven SMAC, Meesters EH, van Duyl FC (2018) Quantification of chemical and mechanical bioerosion rates of six Caribbean excavating sponge species found on the coral reefs of Curaçao. PLoS ONE 13:e0197824. https://doi.org/10.1371/journal.pone.0197824
Deagle BE, Thomas AC, McInnes JC, Clarke LJ, Vesterinen EJ, Clare EL, Kartzinel TR, Eveson JP (2019) Counting with DNA in metabarcoding studies: How should we convert sequence reads to dietary data? Mol Ecol 28:391–406. https://doi.org/10.1111/mec.14734
del Campo J, Pombert J-F, Šlapeta J, Larkum A, Keeling PJ (2017) The ‘other’ coral symbiont: Ostreobium diversity and distribution. ISME J 11:296–299. https://doi.org/10.1038/ismej.2016.101
Dunlap M, Pawlik JR (1998) Spongivory by Parrotfish in Florida Mangrove and Reef Habitats. Mar Ecol 19:325–337. https://doi.org/10.1111/j.1439-0485.1998.tb00471.x
Eggertsen M, Chacin DH, van Lier J, Eggertsen L, Fulton CJ, Wilson S, Halling C, Berkström C (2020) Seascape configuration and fine-scale habitat complexity shape parrotfish distribution and function across a coral reef lagoon. Diversity (basel) 12:391. https://doi.org/10.3390/d12100391
Engelberts JP, Robbins SJ, de Goeij JM, Aranda M, Bell SC, Webster NS (2020) Characterization of a sponge microbiome using an integrative genome-centric approach. ISME J 14:1100–1110. https://doi.org/10.1038/s41396-020-0591-9
Engene N, Tronholm A, Paul VJ (2018) Uncovering cryptic diversity of Lyngbya : the new tropical marine cyanobacterial genus Dapis (Oscillatoriales). J Phycol 54:435–446. https://doi.org/10.1111/jpy.12752
Evans KM, Larouche O, Gartner SM, Faucher RE, Dee SG, Westneat MW (2023) Beaks promote rapid morphological diversification along distinct evolutionary trajectories in Labrid Fishes (Eupercaria: Labridae). Evolution (N Y) qpad115. doi: https://doi.org/10.1093/evolut/qpad115
Ezzat L, Lamy T, Maher RL, Munsterman KS, Landfield KM, Schmeltzer ER, Clements CS, Vega Thurber RL, Burkepile DE (2020) Parrotfish predation drives distinct microbial communities in reef-building corals. Anim Microbiome 2:5. https://doi.org/10.1186/s42523-020-0024-0
Gaino E, Sara M (1994) Siliceous spicules of Tethya seychellensis (Porifera) support the growth of a green alga: a possible light conducting system. Mar Ecol Prog Ser 108:147–152
Goldberg EG, Raab TK, Desalles P, Briggs AA, Dunbar RB, Millero FJ, Woosley RJ, Young HS, Micheli F, Mccauley DJ (2019) Chemistry of the consumption and excretion of the bumphead parrotfish (Bolbometopon muricatum), a coral reef mega-consumer. Coral Reefs 38:347–357. https://doi.org/10.1007/s00338-019-01781-0
Golubic S, Campbell SE (1981) Biogenically Formed Aragonite Concretions in Marine Rivularia. Phanerozoic Stromatolites. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 209–229
González-Resendiz L, Johansen JR, Alba-Lois L, Segal-Kischinevzky C, Escobar-Sánchez V, Jimenez Garcia LF, Hauer T, León-Tejera H (2018) Nunduva, a new marine genus of Rivulariaceae (Nostocales, Cyanobacteria) from marine rocky shores. Fottea 18:86–105. https://doi.org/10.5507/fot.2017.018
Grandcourt EM (2002) Demographic characteristics of a selection of exploited reef fish from the Seychelles: preliminary study. Mar Freshw Res 53:123. https://doi.org/10.1071/MF01123
Guiry MD, Guiry GM (2022) AlgaeBase. World-wide electronic publication. In: National University of Ireland, Galway.
Haberman I, Martone P (2023) Calcified coralline algae have similar caloric value to uncalcified algae. Mar Ecol Prog Ser 713:173–179. https://doi.org/10.3354/meps14341
Hamilton S, Smith J, Price N, Sandin S (2014) Quantifying patterns of fish herbivory on Palmyra Atoll (USA), an uninhabited predator-dominated central Pacific coral reef. Mar Ecol Prog Ser 501:141–155. https://doi.org/10.3354/meps10684
Harris PM, Halley RB, Lukas KJ (1979) Endolith microborings and their preservation in Holocene-Pleistocene (Bahama-Florida) ooids. Geology 7:216. https://doi.org/10.1130/0091-7613(1979)7%3c216:EMATPI%3e2.0.CO;2
Jennings S, Reynolds JD, Polunin NVC (1999) Predicting the Vulnerability of Tropical Reef Fishes to Exploitation with Phylogenies and Life Histories. 13:1466–1475
Johansen JR, González-Resendiz L, Escobar-Sánchez V, Segal-Kischinevzky C, Martínez-Yerena J, Hernández-Sánchez J, Hernández-Pérez G, León-Tejera H (2021) When will taxonomic saturation be achieved? A case study in Nunduva and Kyrtuthrix (Rivulariaceae, Cyanobacteria). J Phycol 57:1699–1720. https://doi.org/10.1111/jpy.13201
Kassambara A (2020) rstatix: Pipe-friendly framework for basic statistical tests.
Kiene WE, Hutchings PA (1994) Bioerosion experiments at Lizard Island, great barrier reef. Coral Reefs 13:91–98. https://doi.org/10.1007/BF00300767
Konstantinou D, Voultsiadou E, Panteris E, Gkelis S (2021) Revealing new sponge-associated cyanobacterial diversity: Novel genera and species. Mol Phylogenet Evol 155:106991. https://doi.org/10.1016/j.ympev.2020.106991
Kramarsky-Winter E, Harel M, Siboni N, Ben DE, Brickner I, Loya Y, Kushmaro A (2006) Identification of a protist-coral association and its possible ecological role. Mar Ecol Prog Ser 317:67–73
Ledlie MH, Graham NAJ, Bythell JC, Wilson SK, Jennings S, Polunin NVC, Hardcastle J (2007) Phase shifts and the role of herbivory in the resilience of coral reefs. Coral Reefs 26:641–653. https://doi.org/10.1007/s00338-007-0230-1
Lloyd Newman JE, Perry CT, Lange ID (2023) Quantifying endolithic bioerosion rates on remote coral reefs in the Central Indian Ocean. Coral Reefs 42:1163–1173. https://doi.org/10.1007/s00338-023-02420-5
Loh T-L, Pawlik JR (2014) Chemical defenses and resource trade-offs structure sponge communities on Caribbean coral reefs. Proc Natl Acad Sci 111:4151–4156. https://doi.org/10.1073/pnas.1321626111
Mallela J, Fox RJ (2018) The role of parrotfishes in the destruction and construction of coral reefs. In: Hoey AS, Bonaldo RM (eds) Biology of Parrotfishes. CRC Press, Bolca Raton, FL, pp 161–196
Marlow J, Schönberg CHL, Davy SK, Haris A, Jompa J, Bell JJ (2019) Bioeroding sponge assemblages: the importance of substrate availability and sediment. J Mar Biol Assoc UK 99:343–358. https://doi.org/10.1017/S0025315418000164
Márquez JC, Zea S (2012) Parrotfish mediation in coral mortality and bioerosion by the encrusting, excavating sponge Cliona tenuis. Mar Ecol 33:417–426. https://doi.org/10.1111/j.1439-0485.2011.00506.x
McMurdie PJ, Holmes S (2013) Phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. https://doi.org/10.1371/journal.pone.0061217
Mortimer C, Dunn M, Haris A, Jompa J, Bell J (2021) Estimates of sponge consumption rates on an Indo-Pacific reef. Mar Ecol Prog Ser 672:123–140. https://doi.org/10.3354/meps13786
Mote S, Schönberg CHL, Samaai T, Gupta V, Ingole B (2019) A new clionaid sponge infests live corals on the west coast of India (Porifera, Demospongiae, Clionaida). Syst Biodivers 17:190–206. https://doi.org/10.1080/14772000.2018.1513430
Nascimento-Silva G, Hardoim CCP, Custódio MR (2022) The Porifera microeukaryome: Addressing the neglected associations between sponges and protists. Microbiol Res 265:127210. https://doi.org/10.1016/j.micres.2022.127210
Nicholson GM (2023) Clements KD (2023b) Fine-scale analysis of substrata grazed by parrotfishes (Labridae:Scarini) on the outer shelf of the Great Barrier Reef. Australia Mar Biol 170:121. https://doi.org/10.1007/s00227-023-04277-2
Nicholson GM, Clements KD (2020) Resolving resource partitioning in parrotfishes (Scarini) using microhistology of feeding substrata. Coral Reefs 39:1313–1327. https://doi.org/10.1007/s00338-020-01964-0
Nicholson GM, Clements KD (2021) Ecomorphological divergence and trophic resource partitioning in 15 syntopic Indo-Pacific parrotfishes (Labridae: Scarini). Biol J Lin Soc 132:590–611. https://doi.org/10.1093/biolinnean/blaa210
Nicholson GM, Clements KD (2022) Scarus spinus, crustose coralline algae and cyanobacteria: an example of dietary specialization in the parrotfishes. Coral Reefs 41:1465–1479. https://doi.org/10.1007/s00338-022-02295-y
Nicholson GM, Clements KD (2023) Micro-photoautotroph predation as a driver for trophic niche specialization in 12 syntopic Indo-Pacific parrotfish species. Biological J Linnean Soc. https://doi.org/10.1093/biolinnean/blad005/7115621
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P (2019) Vegan: community ecology package. R Package Ver 2:5–6
Ong L, Holland KN (2010) Bioerosion of coral reefs by two Hawaiian parrotfishes: species, size differences and fishery implications. Mar Biol 157:1313–1323. https://doi.org/10.1007/s00227-010-1411-y
Pawlik JR, Loh T-L, Mcmurray SE (2018) A review of bottom-up vs. top-down control of sponges on Caribbean fore-reefs: what’s old, what’s new, and future directions. Peer J. 6:e4343. https://doi.org/10.7717/peerj.4343
Pentecost A, Franke U (2010) Photosynthesis and calcification of the stromatolitic freshwater cyanobacterium Rivularia. Eur J Phycol 45:345–353. https://doi.org/10.1080/09670262.2010.492914
Pernice M, Raina J-B, Rädecker N, Cárdenas A, Pogoreutz C, Voolstra CR (2020) Down to the bone: the role of overlooked endolithic microbiomes in reef coral health. ISME J 14:325–334. https://doi.org/10.1038/s41396-019-0548-z
Perry CT, Lange ID, Stuhr M (2023) Quantifying reef-derived sediment generation: Introducing the SedBudget methodology to support tropical coastline and island vulnerability studies. Cambridge Prisms: Coastal Futures 1:e26. https://doi.org/10.1017/cft.2023.14
Podell S, Blanton JM, Oliver A, Schorn MA, Agarwal V, Biggs JS, Moore BS, Allen EE (2020) A genomic view of trophic and metabolic diversity in clade-specific Lamellodysidea sponge microbiomes. Microbiome 8:97. https://doi.org/10.1186/s40168-020-00877-y
Pronzato R, Manconi R (2008) Mediterranean commercial sponges: over 5000 years of natural history and cultural heritage. Mar Ecol 29:146–166. https://doi.org/10.1111/j.1439-0485.2008.00235.x
R Core Development Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Radtke G, Golubic S (2011) Microbial Euendolithic Assemblages and Microborings in Intertidal and Shallow Marine Habitats: Insight in Cyanobacterial Speciation. In: Reitner J, Quéric N-V, Arp G (eds) Advances in stromatolite geobiology. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 233–263
Ramsby BD, Hill MS, Thornhill DJ, Steenhuizen SF, Achlatis M, Lewis AM, LaJeunesse TC (2017) Sibling species of mutualistic Symbiodinium clade G from bioeroding sponges in the western Pacific and western Atlantic oceans. J Phycol 53:951–960. https://doi.org/10.1111/jpy.12576
Renema W, Pandolfi JM, Kiessling W, Bosellini FR, Klaus JS, Korpanty C, Rosen BR, Santodomingo N, Wallace CC, Webster JM, Johnson KG (2016) Are coral reefs victims of their own past success? Sci Adv 2:e1500850. https://doi.org/10.1126/sciadv.1500850
Rützler K (1990) Associations between caribbean sponges and photosynthetic organisms. In: Rützler K (ed) New perspectives in sponge biology. Smithsonian Institution Press, Washington, D.C., p 533
Rützler K (2002) Impact of crustose clionid sponges on caribbean reef corals. Acta Geologica Hispanica 37:61–72
Schönberg CHL (2002) Substrate effects on the bioeroding demosponge Cliona orientalis. 1 Bioerosion Rates. Marine Ecol 23:313–326. https://doi.org/10.1046/j.1439-0485.2002.02811.x
Strunecký O, Ivanova AP, Mareš J (2023) An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis. J Phycol 59:12–51. https://doi.org/10.1111/jpy.13304
Tan MH, Loke S, Croft LJ, Gleason FH, Lange L, Pilgaard B, Trevathan-Tackett SM (2021) First genome of Labyrinthula sp., an opportunistic seagrass pathogen, reveals novel insight into marine protist phylogeny, ecology and CAZyme cell-wall degradation. Microb Ecol 82:498–511. https://doi.org/10.1007/s00248-020-01647-x/Published
Taylor BM, Pardee C (2017) Growth and maturation of the redlip parrotfish Scarus rubroviolaceus. J Fish Biol 90:2452–2461. https://doi.org/10.1111/jfb.13309
Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347
Tebbett SB, Bennett S, Bellwood DR (2023) A functional perspective on the meaning of the term ‘herbivore’: patterns versus processes in coral reef fishes. Coral Reefs. https://doi.org/10.1007/s00338-023-02378-4
Titlyanov AE, Titlyanova VT, Li X, Huang H (2017) Coral reef marine plants of Hainan island. Academic Press, London
Tribollet A, Langdon C, Golubic S, Atkinson M (2006) Endolithic microflora are major primary producers in dead carbonate substrates of Hawaiian coral reefs. J Phycol 42:292–303. https://doi.org/10.1111/j.1529-8817.2006.00198.x
Tribollet A, Golubic S (2011) Reef bioerosion: Agents and processes. In: Coral Reefs: An Ecosystem in Transition. pp 435–449
Usher KM (2008) The ecology and phylogeny of cyanobacterial symbionts in sponges. Mar Ecol 29:178–192. https://doi.org/10.1111/j.1439-0485.2008.00245.x
van den Hoek C, Cortel-Breeman AM, Wanders JBW (1975) Algal zonation in the fringing coral reef of curaçao, Netherlands antilles, in relation to zonation of corals and gorgonians. Aquat Bot 1:269–308. https://doi.org/10.1016/0304-3770(75)90028-5
van Duyl FC, Moodley L, Nieuwland G, van Ijzerloo L, van Soest RWM, Houtekamer M, Meesters EH, Middelburg JJ (2011) Coral cavity sponges depend on reef-derived food resources: stable isotope and fatty acid constraints. Mar Biol 158:1653–1666. https://doi.org/10.1007/s00227-011-1681-z
Vergeer LHT, Den Hartog C (1994) Omnipresence of Labyrinthulaceae in seagrasses. Aquat Bot 48:1–20
Wainwright PC, Price SA (2018) Innovation and diversity of the feeding mechanism in parrotfishes. In: Hoey AS, Bonaldo RM (eds) Biology of parrotfishes. CRC Press, Boca Raton, FL, pp 26–41
Wang Q, Ye H, Xie Y, He Y, Sen B, Wang G (2019) Culturable diversity and lipid production profile of Labyrinthulomycete protists isolated from coastal mangrove habitats of China. Mar Drugs 17:268. https://doi.org/10.3390/md17050268
Webster NS, Thomas T (2016) The Sponge Hologenome. Mbio. https://doi.org/10.1128/mBio.00135-16
Wiebe WJ, Johannes RE, Webb KL (1975) Webb KL Nitrogen fixation in a coral reef community. Science (1979). https://doi.org/10.1126/science.188.4185.257
Wulff JL (2021) Targeted predator defenses of sponges shape community organization and tropical marine ecosystem function. Ecol Monogr 91:1–29
Wyness AJ, Roush D, McQuaid CD (2022) Global distribution and diversity of marine euendolithic cyanobacteria. J Phycol 58:746–759. https://doi.org/10.1111/jpy.13288
Yarlett RT, Perry CT, Wilson RW (2021) Quantifying production rates and size fractions of parrotfish-derived sediment: A key functional role on Maldivian coral reefs. Ecol Evol 11:16250–16265. https://doi.org/10.1002/ece3.8306
Acknowledgements
We would like to thank: Anne Hoggett and Lyle Vail at the Lizard Island Research Station, Paul Kench for help developing our coring technique and advice on coral reef taphonomy, Adrian Turner for assistance with microscopy and Howard Choat for ongoing support. Great thanks to Judy Sutherland and Wendy Nelson for advice on DNA extraction techniques for crustose coralline algae. Also thanks to Alessandro Pisaniello for practical guidance on DNA extraction and to Viv Ward for her clipart. We acknowledge the use of New Zealand eScience Infrastructure (NeSI) high performance computing facilities.
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Funding was provided by the University of Auckland School of Biological Sciences Performance Based Research Fund and University of Auckland Doctoral Scholarship.
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Both authors contributed to the study conception, design and fieldwork. G.M.N carried out the laboratory work, bioinformatics and analysis and led the writing of the manuscript. K.D.C. critically reviewed the versions of the manuscript. Both authors read and approved the final manuscript.
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Reef sampling was conducted under the Lizard Island Research Permit granted by Great Barrier Reef Marine Park Authority (GBRMPA; permit no. G14/36625.1). Fish were observed in their natural habitat and no fish were killed or injured during data collection for this study.
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Nicholson, G.M., Clements, K.D. A role for encrusting, endolithic sponges in the feeding of the parrotfish Scarus rubroviolaceus? Evidence of further trophic diversification in Indo-Pacific Scarini. Coral Reefs (2024). https://doi.org/10.1007/s00338-024-02482-z
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DOI: https://doi.org/10.1007/s00338-024-02482-z