Abstract
Habitat availability underpins the diversity and distribution of benthic marine communities. Sponges are significant structural components of seabeds; therefore, understanding sponge-community associations are important for the effective management of marine biodiversity. Invertebrate communities were quantified from 11 sponge species having distinct morphologies from Ningaloo Reef (tropical) and Rottnest Island (temperate), Western Australia. Communities from substrate adjacent to sponges were additionally sampled for comparisons to sponge-associated fauna. Gross and fine-scale morphological features of sponge host species were quantified to assess their effects on faunal abundance and diversity. A total of 3966 individuals from 125 taxa were extracted, showing low co-occurrences of taxa from both sponges and the surrounding substrate (Ningaloo 8.9%; Rottnest 11.2%). Four out of the 11 sponges supported higher fauna abundance compared to their surrounding substrate, including Haliclona sp. NTM148 (Ningaloo; 1.21 ± 0.54 N.cm−3, 60 × higher than substrate) and Monanchora clathrata (Rottnest; 2.87 ± 1.7 N.cm−3, 32 × higher than substrate). These communities were dominated by the barnacle Acastinae sp.4 (100%) and sedentary polychaete Spionidae sp. 1 (99%), respectively, highlighting strong host-specific associations. Sponge size (volume), % of internal space, minimum diameter of internal space, and gross morphological complexity were important at explaining variation in faunal assemblage, with larger sponges having more internal space of larger minimum canal diameter supporting higher community abundance. This study highlights the significance of large and long-lived sponges as sources of unique marine biodiversity that are yet to be discovered and the importance of sponge gardens for the conservation of cryptic marine biodiversity.
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References
Abdo DA (2007) Endofauna differences between two temperate marine sponges (Demospongiae; Haplosclerida; Chalinidae) from southwest Australia. Mar Biol 152:845–854. https://doi.org/10.1007/s00227-007-0736-7
Amsler MO, Mcclintock JB, Amsler CD, Angus RA, Baker BJ (2009) An evaluation of sponge-associated amphipods from the Antarctic Peninsula. Antarct Sci 21(6):579. https://doi.org/10.1017/S0954102009990356
Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth
Araujo RM, Bartsch I, Bekkby T, Erzini K, Sousa-Pinto I (2013) What is the impact of kelp forest density and/or area on fisheries? Environ Evid 2:15. https://doi.org/10.1186/2047-2382-2-15
Ávila E, Ortega-Bastida AL (2015) Influence of habitat and host morphology on macrofaunal assemblages associated with the sponge Halichondria melanadocia in an estuarine system of the southern Gulf of Mexico. Mar Ecol 36(4):1345–1353. https://doi.org/10.1111/maec.12233
Bakus GJ, Targett NM, Schulte B (1986) Chemical ecology of marine organisms: an overview. J Chem Ecol 12:951–987. https://doi.org/10.1007/BF01638991
Beepat SS, Appadoo C, Marie DEP, Paula JPM, Çinar ME, Sivakumar K (2014) Macrofauna associated with the sponge Neopetrosia exigua (Kirkpatrick, 1900) from Mauritius. West Indian Ocean J Mar Sci 13:133–142
Bell JJ, Bennett HM, Rovellini A, Webster NS (2018) Sponges to be winners under near-future climate scenarios. Bioscience 68:955–968. https://doi.org/10.1093/biosci/biy142
Cerrano C, Calcinai B, Pinca S, Bavestrello G (2006) Reef sponges as hosts of biodiversity: cases from North Sulawesi. In Xth Coral Reef Symposium, Okinawa, pp 208–213
Chanas B, Pawlik JR (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
Clarke K, Gorley R (2015) Getting started with PRIMER v7. PRIMER-E: Plymouth, Plymouth Marine Laboratory
de Goeij JM, van Oevelen D, Vermeij MJ, Osinga R, Middelburg JJ, de Goeij AF, Admiraal W (2013) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342:108–110. https://doi.org/10.1126/science.1241981
Díaz MC, Rützler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69:535–546
Duarte L, Nalesso R (1996) The sponge Zygomycale parishii (Bowerbank) and its endobiotic fauna. Estuar Coast Shelf Sci 42:139–151. https://doi.org/10.1006/ecss.1996.0011
Duffy JE (1996) Eusociality in a coral-reef shrimp. Nature 381:512. https://doi.org/10.1038/381512a0
Fiore CL, Jutte PC (2010) Characterization of macrofaunal assemblages associated with sponges and tunicates collected off the southeastern United States. Invertebr Biol 129:105–120. https://doi.org/10.1111/j.1744-7410.2010.00184.x
Frith DW (1976) Animals associated with sponges at North Hayling, Hampshire. Zool J Linn Soc 58:353–362. https://doi.org/10.1111/j.1096-3642.1976.tb01005.x
Fromont J, Abdul Wahab M, Gomez O, Ekins M, Grol M, Hooper J (2016) Patterns of sponge biodiversity in the pilbara. Northwest Aust Divers. https://doi.org/10.3390/d8040021
García-Hernández JE, Hammerman NM, Cruz-Motta JJ, Schizas NV (2019) Associated organisms inhabiting the calcareous sponge Clathrina lutea in La Parguera. Puerto Rico Caribb J Sci 49(2–3):239–254. https://doi.org/10.18475/cjos.v49i2.a12
Heyward A, Fromont J, Schoenberg C, Colquhoun J, Radford B, Gomez O (2010) The sponge gardens of Ningaloo reef, Western Australia. Open Mar Biol J 4:3–11. https://doi.org/10.2174/1874450801004010003
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83. https://doi.org/10.1126/science.aan8048
Ilan M, Ben-Eliahu MN, Galil B (1994) Three deep water sponges from the eastern Mediterranean and their associated fauna. Ophelia 39(1):45–54. https://doi.org/10.1080/00785326.1994.10429901
Ilan M, Loya Y, Kolbasov G, Brickner I (1999) Sponge-inhabiting barnacles on Red Sea coral reefs. Mar Biol 133:709–716. https://doi.org/10.1007/s002270050512
Jackson J, Buss L (1975) Alleopathy and spatial competition among coral reef invertebrates. PNAS 72:5160–5163. https://doi.org/10.1073/pnas.72.12.5160
Kerry J, Bellwood D (2012) The effect of coral morphology on shelter selection by coral reef fishes. Coral Reefs 31:415–424. https://doi.org/10.1007/s00338-011-0859-7
Kersken D, Göcke C, Brandt A, Lejzerowicz F, Schwabe E, Seefeldt MA, Veit-Köhler JD (2014) The infauna of three widely distributed sponge species (Hexactinellida and Demospongiae) from the deep Ekström Shelf in the Weddell Sea, Antarctica. Deep Sea Res Part II 108:101–112. https://doi.org/10.1016/j.dsr2.2014.06.005
Klitgaard AB (1995) The fauna associated with outer shelf and upper slope sponges (Porifera, Demospongiae) at the Faroe Islands, northeastern Atlantic. Sarsia 80:1–22. https://doi.org/10.1080/00364827.1995.10413574
Koukouras A, Voultsiadou-Koukoura E, Chintiroglou H, Dounos C (1985) Benthic bionomy of the North Aegean Sea lll. A comparison of the macobenthic animal assemblages associated with seven sponge species. Cah Biol Mar 26:301–319
Koukouras A, Russo A, Voultsiadou-Koukoura E, Dounas C, Chintiroglou C (1992) Relationship of sponge macrofauna with the morphology of their hosts in the North Aegean Sea. Int Rev Ges Hydrobiol Hydrogr 77:609–619. https://doi.org/10.1002/iroh.19920770406
Koukouras A, Russo A, Voultsiadou-Koukoura E, Arvanitidis C, Stefanidou D (1996) Macrofauna associated with sponge species of different morphology. Mar Ecol 17:569–582. https://doi.org/10.1111/j.1439-0485.1996.tb00418.x
Kubanek J, Whalen KE, Engel S, Kelly SR, Henkel TP, Fenical W, Pawlik JR (2002) Multiple defensive roles for triterpene glycosides from two Caribbean sponges. Oecologia 131:125–136. https://doi.org/10.1007/s00442-001-0853-9
Lattig P, Martin D (2011) Sponge-associated Haplosyllis (Polychaeta: Syllidae: Syllinae) from the Caribbean Sea, with the description of four new species. Sci Mar 75(4):733–758. https://doi.org/10.3989/scimar.2011.75n4733
Lemloh ML, Fromont J, Brummer F, Usher KM (2009) Diversity and abundance of photosynthetic sponges in temperate Western Australia. BMC Ecol 9:4. https://doi.org/10.1186/1472-6785-9-4
Lesser MP, Mueller B, Pankey MS, Macartney KJ, Slattery M, de Goeij JM (2019) Depth-dependent detritus production in the sponge Halisarca caerulea. Limnol Oceanogr 65(6):1200–1216. https://doi.org/10.1002/lno.11384
Maldonado M, Aguilar R, Bannister RJ, Bell JJ, Conway KW, Dayton PK, Díaz C, Gutt J, Kelly M, Kenchington EL (2017) Sponge grounds as key marine habitats: a synthetic review of types, structure, functional roles, and conservation concerns. In: Rossi S, Bramanti L, Gori A, Orejas C (eds) Marine animal forests: the ecology of benthic biodiversity hotspots, pp 145–183. https://doi.org/10.1007/978-3-319-21012-4_24
Musco L, Giangrande A (2005) A new sponge-associated species, Syllis mayerin. sp.(Polychaeta: Syllidae), with a discussion on the status of S. armillaris (Müller, 1776). Sci Mar 69(4):467–474. https://doi.org/10.3989/scimar.2005.69n4467
Myers AA, George AM (2017) Amphipoda living in sponges on the Great Barrier Reef, Australia (Crustacea, Amphipoda). Zootaxa 4365(5):571–584. https://doi.org/10.11646/zootaxa.4365.5.4
Neves G, Omena E (2003) Influence of sponge morphology on the composition of the polychaete associated fauna from Rocas Atoll, northeast Brazil. Coral Reefs 22:123–129. https://doi.org/10.1007/s00338-003-0295-4
Padua A, Lanna E, Klautau M (2016) Macrofauna inhabiting the sponge Paraleucilla magna (Porifera: Calcarea) in Rio de Janeiro, Brazil. J Mar Biolog Assoc UK 96(3):605. https://doi.org/10.1017/S0025315412000434
Pawlik JR, McMurray SE (2019) The emerging ecological and biogeochemical importance of sponges on coral reefs. Annu Rev Mar Sci 12:315–337. https://doi.org/10.1146/annurev-marine-010419-010807
Ribeiro SM, Omena EP, Muricy G (2003) Macrofauna associated to Mycale microsigmatosa (Porifera, Demospongiae) in Rio de Janeiro State, SE Brazil. Estuar Coast Shelf Sci 57:951–959. https://doi.org/10.1016/S0272-7714(02)00425-0
Rix L, de Goeij JM, van Oevelen D, Struck U, Al-Horani FA, Wild C, Naumann MS (2018) Reef sponges facilitate the transfer of coral-derived organic matter to their associated fauna via the sponge loop. Mar Ecol Prog Ser 589:85–96. https://doi.org/10.3354/meps12443
Roberts D, Davis A (1996) Patterns in sponge (Porifera) assemblages on temperate coastal reefs off Sydney, Australia. Mar Freshw Res 47:897–906. https://doi.org/10.1071/MF9960897
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676. https://doi.org/10.1038/nmeth.2072
Schönberg CHL, Fromont J (2011) Sponge gardens of Ningaloo Reef (Carnarvon Shelf, Western Australia) are biodiversity hotspots. Hydrobiologia 687:143–161. https://doi.org/10.1007/978-94-007-4688-6_13
Schönberg C, Fromont J (2014) Sponge functional growth forms as a means for classifying sponges without taxonomy. The Ningaloo Atlas Available at https://eatlas.org.au/node/33141 (Accessed 5 April 2019)
Skilleter GA, Russell BD, Degnan BM, Garson MJ (2005) Living in a potentially toxic environment: comparisons of endofauna in two congeneric sponges from the Great Barrier Reef. Mar Ecol Prog Ser 304:67–75. https://doi.org/10.3354/meps304067
Sorokin S, Fromont J, Currie D (2007) Demosponge biodiversity in the benthic protection zone of the Great Australian Bight. T Roy Soc South Aust 131:192–204. https://doi.org/10.1080/03721426.2007.10887083
Stella JS, Jones GP, Pratchett MS (2010) Variation in the structure of epifaunal invertebrate assemblages among coral hosts. Coral Reefs 29:957–973. https://doi.org/10.1007/s00338-010-0648-8
Tsubaki R, Kato M (2014) A novel filtering mutualism between a sponge host and its endosymbiotic bivalves. PLoS ONE 9:e108885. https://doi.org/10.1371/journal.pone.0108885
Van Syoc RJ, Van Soest RW, Xavier JR, Hooper JN (2015) A phylogenetic overview of sponge-inhabiting barnacles and their host specificity (Crustacea, Cirripedia). Proc Calif Acad Sci 4:331–357
Veal CJ, Holmes G, Nunez M, Hoegh-Guldberg O, Osborn J (2010) A comparative study of methods for surface area and three-dimensional shape measurement of coral skeletons. Limnol Oceanogr-Meth 8(5):241–253. https://doi.org/10.4319/lom.2010.8.241
Villamizar E, Laughlin R (1991) Fauna associated with the sponges Aplysina archeri and Aplysina lacunosa in a coral reef of the Archipielago de Los Roques, National Park, Venezuela. In: Reitner J, Keupp H (eds) Fossil and recent sponges. Springer, Berlin, Heidelberg, pp 522–542. https://doi.org/10.1007/978-3-642-75656-6_44
Westinga EPHC, Hoetjes PC (1981) The intrasponge fauna of Spheciospongia vesparia (Porifera, Demospongiae) at Curaçao and Bonaire. Mar Biol 62(2–3):39–150. https://doi.org/10.1007/BF00388176
Wulff JL (2006) Ecological interactions of marine sponges. Can J Zool 84:146–166. https://doi.org/10.1139/z06-019
Yu M-C, Kolbasov GA, Hosie AM, Lee T-M, Chan BK (2017) Descriptions of four new sponge-inhabiting barnacles (Thoracica: Archaeobalanidae: Acastinae). Zootaxa 4277:151–198. https://doi.org/10.11646/zootaxa.4277.2.1
Acknowledgements
We would like to thank the Master and crew of the Australian Institute of Marine Science RV Solander for facilitating fieldwork and sample collections at Ningaloo Reef. Thank you to Nick Thake and John Statton for field assistance at Ningaloo Reef and Rottnest Island, respectively. We would also to thank Belinda Alvarez for formally identifying the sponges used in this study. Collections were performed under permits provided by the Western Australian Department of Parks and Wildlife and Western Australian Fisheries, DPaW SF010984, WA Fisheries Exemption 2885 and WA Fisheries Exemption 3021. YYC was supported by a full scholarship for her MSc from the Ministry of Education of Taiwan. We would like to thank the Associate Editor and 4 Reviewers who all provided helpful comments to improve the manuscript.
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YYC was supported by a full scholarship from the Ministry of Education of Taiwan. The research was partly funded by the Australian Institute of Marine Science.
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Y-YC conducted field and lab work, and statistical analyses, and drafted the manuscript, JP and GK contributed to the draft of the manuscript, MAAW conceived the project, conducted field and lab work, statistical analyses, and drafted the manuscript.
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This research was conducted in accordance with the University of Western Australia’s policies, procedures, and guidelines. No specific permissions were required. Collections were performed under permits provided by the Western Australian Department of Parks and Wildlife and Western Australian Fisheries, DPaW SF010984, WA Fisheries Exemption 2885 and WA Fisheries Exemption 3021.
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Chin, YY., Prince, J., Kendrick, G. et al. Sponges in shallow tropical and temperate reefs are important habitats for marine invertebrate biodiversity. Mar Biol 167, 164 (2020). https://doi.org/10.1007/s00227-020-03771-1
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DOI: https://doi.org/10.1007/s00227-020-03771-1