Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5318 No. 2: 19 Jul. 2023
Type: Article
Published: 2023-07-19
DOI: 10.11646/zootaxa.5318.2.1
Page range: 151-194
Abstract views: 925
PDF downloaded: 37

The Sponges of the Carmel Pinnacles Marine Protected Area

Ecology; Evolution; and Marine Biology Department; University of California; Santa Barbara; Monterey Bay National Marine Sanctuary; National Ocean Service; NOAA; Santa Cruz; California; USA
Monterey Bay National Marine Sanctuary; National Ocean Service; NOAA; Santa Cruz; California; USA
Porifera Sponges Carmel Pinnacles Marine Protected Area

Abstract

California's network of marine protected areas was created to protect the diversity and abundance of native marine life, but the status of some taxa is very poorly known. Here we describe the sponges (phylum Porifera) from the Carmel Pinnacles State Marine Reserve, as assessed by a SCUBA-based survey in shallow waters. Of the 29 sponge species documented, 12 (41%) of them were previously unknown. Using a combination of underwater photography, DNA sequencing, and morphological taxonomy, we greatly improve our understanding of the status and distribution of previously described species and formally describe the new species as Hymedesmia promina sp. nov., Phorbas nebulosus sp. nov., Clathria unoriginalis sp. nov., Clathria rumsena sp. nov., Megaciella sanctuarium sp. nov., Mycale lobos sp. nov., Xestospongia ursa sp. nov., Haliclona melissae sp. nov., Halichondria loma sp. nov., Hymeniacidon fusiformis sp. nov., Scopalina carmela sp. nov., and Obruta collector gen. nov., sp. nov. An additional species, Lissodendoryx topsenti (de Laubenfels 1930), is moved to Hemimycale, and H. polyboletus comb. nov., nom. nov. is created due to preoccupation by H. topsenti (Burton, 1929). Several of the new species appear to be rare and/or have very restricted distributions, as they were not found at comparative survey sites outside of Carmel Bay. These results illustrate the potential of qualitative presence/absence systematic surveys of understudied taxa to discover and document substantial novel diversity.

 

References

  1. Ackers, R.G., Moss, D., Picton, B.E., Stone, S.M.K. & Morrow, C.C. (2007) Sponges of the British Isles: A color guide and working document. Marine Conservation Society, Ross-on-Wye, 156 pp.
  2. Aguilar-Camacho, J.M. & Carballo, J.L. (2012) New and little-known Poecilosclerid sponges from the Mexican Pacific Ocean. Zoological Studies, 51, 1139–1153.
  3. Aguilar-Camacho, J.M. & Carballo, J.L. (2013) Raspailiidae (Porifera: Demospongiae: Axinellida) from the Mexican Pacific Ocean with the description of seven new species. Journal of Natural History, 47, 25–28. https://doi.org/10.1080/00222933.2013.769642
  4. Austin, W.C. (1985) An Annotated Checklist of Marine Invertebrates in the Cold Temperate Northeast Pacific. Volume 1. Khoyatan Marine Laboratory, Cowichan Bay, British Columbia, 43 pp.
  5. Bakus, G.J. (1966) Marine poeciloscleridan sponges of the San Juan Archipelago, Washington. Journal of Zoology, 149, 415–531. https://doi.org/10.1111/j.1469-7998.1966.tb02994.x
  6. Bakus, G.J. & Green, K.D. (1987) The distribution of marine sponges collected from the 1976-1978 Bureau of Land Management Southern California Bight program. Bulletin of the Southern California Academy of Sciences, 86, 57–88.
  7. Bell, J.J. (2008) The functional roles of marine sponges. Estuarine, Coastal and Shelf Science, 79, 341–353. https://doi.org/10.1016/j.ecss.2008.05.002
  8. Blanchette, C., Miner, C., Raimondi, P., Lohse, D., Heady, K. & Broitman, B. (2008) Biogeographical patterns of rocky intertidal communities along the Pacific coast of North America. Journal of Biogeography, 35, 1593–1607. https://doi.org/10.1111/j.1365-2699.2008.01913.x
  9. Bowerbank, J.S. (1866) A Monograph of the British Spongiadae. Vol. 2. Ray Society, London, 388 pp. [https://biodiversitylibrary.org/page/1905089]
  10. Bowerbank, J.S. (1874) A Monograph of the British Spongiadae. Vol. 3. Ray Society, London, 367 pp.
  11. Burton, M. (1929) Porifera. Part II. Antarctic sponges. British Antarctic ('Terra Nova’) Expedition, 1910. Natural History Report, London, Zoology, 6, 393–458.
  12. Carballo, J.L. & Cruz-Barraza, J.A. (2008) First record of Axinyssa Lendenfeld, 1897 (Demospongiae, Halichondrida) from the East Pacific Ocean, with the description of Axinyssa isabela sp. nov. Zootaxa, 1784 (1), 58–68. https://doi.org/10.11646/zootaxa.1784.1.4
  13. Carballo, J.L. & Cruz-Barraza, J.A. (2010) A revision of the genus Mycale (Poecilosclerida: Mycalidae) from the Mexican Pacific Ocean. Contributions to Zoology, 79, 165–191. https://doi.org/10.1163/18759866-07904003
  14. Carballo, J.L., Cruz-Barraza, J.A. & Patricia, G. (2004) Taxonomy and description of clionaid sponges (Hadromerida, Clionaidae) from the Pacific Ocean of Mexico. Zoological Journal of the Linnean Society, 141, 353–397. https://doi.org/10.1111/j.1096-3642.2004.00126.x
  15. Chombard, C., Boury-Esnault, N. & Tillier, S. (1998) Reassessment of homology of morphological characters in tetractinellid sponges based on molecular data. Systematic Biology, 47, 351–366. https://doi.org/10.1080/106351598260761
  16. De Weerdt, W.H. (2002) Family Chalinidae Gray, 1867. In: Hooper, J.N.A. & van Soest, R.W.M. (Eds.), Systema Porifera. A guide to the classification of sponges. Kluwer Academic/Plenum Publ., New York, New York, pp. 852–873. https://doi.org/10.1007/978-1-4615-0747-5_91
  17. Desqueyroux-Faúndez, R. & van Soest, R.W.M. (1997) Shallow-water Demosponges of the Galapagos Islands. Revue suisse de Zoologie, 104, 379–467. https://doi.org/10.5962/bhl.part.80003
  18. Desqueyroux-Faúndez, R. & Valentine, C. (2002) Family Petrosiidae Van Soest, 1980. In: Hooper, J.N.A. & van Soest, R.W.M. (Eds.), Systema Porifera: A Guide to the Classification of Sponges. Kluwer Academic/Plenum Publ., New York, New York, pp. 906–917. https://doi.org/10.1007/978-1-4615-0747-5_95
  19. Dickinson, M.G. (1945) Sponges of the Gulf of California. In: Reports on the collections obtained by Allan Hancock Pacific Expeditions of Velero III off the coast of Mexico, Central America, South America, and Galapagos Islands in 1932, in 1933, in 1934, in 1935, in 1936, in 1937, in 1939, and 1940. The University of Southern California Press, Los Angeles, California, pp. 1–55.
  20. Duchassaing de Fonbressin, P. & Michelotti, G. (1864) Spongiaires de la mer Caraibe. Natuurkundige verhandelingen van de Hollandsche maatschappij der wetenschappen te Haarlem, 21, 1–124.
  21. Folmer, O., Black, M., Wr, H. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial Cytochrome C oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.
  22. Gazave, E., Carteron, S., Chenuil, A., Richelle-Maurer, E., Boury-Esnault, N. & Borchiellini, C. (2010) Polyphyly of the genus Axinella and of the family Axinellidae (Porifera: Demospongiae). Molecular Phylogenetics and Evolution, 57, 35–47. https://doi.org/10.1016/j.ympev.2010.05.028
  23. de Goeij, J.M., van Oevelen, D., Vermeij, M.J.A., Osinga, R., Middelburg, J.J., de Goeij, A.F.P.M. & 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
  24. Goodwin, C.E., Berman, J. & Hendry, K.R. (2019) Demosponges from the sublittoral and shallow-circalittoral (<24m depth) Antarctic Peninsula with a description of four new species and notes on in situ identification characteristics. Zootaxa, 4658 (3), 461–508. https://doi.org/10.11646/zootaxa.4658.3.3
  25. Green, K.D. & Bakus, G.J. (1994) Taxonomic atlas of the benthic marine fauna of the Western Santa Maria Basin and the Western Santa Barbara Channel. Vol. 2. The Porifera. The Santa Barbara Museum of Natural History, Santa Barbara, California, 82 pp.
  26. Hajdu, E. & Desqueyroux-Faúndez, R. (1994) A synopsis of South American Mycale (Mycale) (Poecilosclerida, Demospongiae), with description of three new species and a cladistic analysis of Mycalidae. Revue Suisse de Zoologie, 101, 563–600. https://doi.org/10.5962/bhl.part.79918
  27. Hartman, W.D. (1975) Phylum Porifera. In: Smith, R.I. & Carlton, J.T. (Eds.), Light’s Manual: Intertidal Invertebrates of the Central California Coast. 3rd Edition. University of California Press, Berkeley, California, pp. 32–64.
  28. Hoang, D., Chernomor, O., von Haeseler, A., Minh, B. & Vinh, L. (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35, 518–522. https://doi.org/10.1093/molbev/msx281
  29. Hooper, J.N.A. (2002a) Family Acarnidae Dendy, 1922. In: Hooper, J.N.A. & van Soest, R.W.M. (Eds.), Systema Porifera. A Guide to the Classification of Sponges. Kluwer Academic/Plenum Publ., New York, New York, pp. 412–431. https://doi.org/10.1007/978-1-4615-0747-5_51
  30. Hooper, J.N.A. (2002b) Family Microcionidae Carter, 1875. In: Hooper, J.N.A. & van Soest, R.W.M. (Eds.), Systema Porifera: A Guide to the Classification of Sponges. Springer, Boston, pp. 432–468. https://doi.org/10.1007/978-1-4615-0747-5_52
  31. Hooper, J.N.A., Lehnert, H. & Zea, S. (1999) Revision of Aulospongus Norman and review of Raspailiidae with rhabdostyles (Porifera: Demospongiae). Memoirs of the Queensland Museum, 43, 649–708.
  32. Ilan, M., Ben-Eliahu, M.N. & Galil, B. (1994) Three deep water sponges from the Eastern Mediterranean and their associated Fauna. Ophelia, 39, 45–54. https://doi.org/10.1080/00785326.1994.10429901
  33. Katoh, K., Rozewicki, J. & Yamada, K.D. (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20, 1160–1166. https://doi.org/10.1093/bib/bbx108
  34. Klontz, S.W. (1989) Ecology and systematics of the intertidal sponges of Southeast Farallon Island. Masters, San Francisco State University, San Francisco, California.
  35. Koltun, V.M. (1958) Cornacuspongia of sea waters washing the South Sakhalin and the South Kurile Island region. Issledovaniya dal’nevostochnÿkh morei SSR, 5, 42–77.
  36. Lambe, L.M. (1895) Sponges from the Western Coast of North America. Transactions of the Royal Society of Canada, 12, 113–138.
  37. de Laubenfels, M.W. (1927) The red sponges of Monterey Peninsula, California. Annals and Magazine of Natural History, Series 9, 19 (110), 258–266. https://doi.org/10.1080/00222932708633594
  38. de Laubenfels, M.W. (1930) The Sponges of California. Stanford University Bulletin, 5, 24–29.
  39. de Laubenfels, M.W. (1932) The marine and fresh-water sponges of California. Proceedings of the United States National Museum, 81, 1–140. https://doi.org/10.5479/si.00963801.81-2927.1
  40. Lee, W., Elvin, D. & Reiswig, H. (2007) The sponges of California: A guide and key to the marine sponges of California. Monterey Bay Sanctuary Foundation, Monterey, California, 395 pp.
  41. Lehnert, H., Stone, R. & Heimler, W. (2006) New species of Poecilosclerida (Demospongiae, Porifera) from the Aleutian Islands, Alaska, USA. Zootaxa, 1155 (1), 1–23. https://doi.org/10.11646/zootaxa.1155.1.1
  42. Letunic, I. & Bork, P. (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Research, 47, W256–W259. https://doi.org/10.1093/nar/gkz239
  43. Lonhart, S.I., Jeppesen, R., Beas-Luna, R., Crooks, J.A. & Lorda, J. (2019) Shifts in the distribution and abundance of coastal marine species along the eastern Pacific Ocean during marine heatwaves from 2013 to 2018. Marine Biodiversity Records, 12, 13. https://doi.org/10.1186/s41200-019-0171-8
  44. Lundbeck, W. (1910) Porifera. (Part III.) Desmacidonidae. Bianco Luno, Copenhagen.
  45. Mikkelsen, P.M. & Cracraft, J. (2001) Marine biodiversity and the need for systematic inventories. Bulletin of Marine Science, 69, 525–534.
  46. Montagu, G. (1818) An Essay on Sponges, with Descriptions of all the Species that have been discovered on the Coast of Great Britain. Memoirs of the Wernerian Natural History Society, 2, 67–122.
  47. Morrow, C. & Cárdenas, P. (2015) Proposal for a revised classification of the Demospongiae (Porifera). Frontiers in Zoology, 12, 1–27. https://doi.org/10.1186/s12983-015-0099-8
  48. Morrow, C.C., Picton, B.E., Erpenbeck, D., Boury-Esnault, N., Maggs, C.A. & Allcock, A.L. (2012) Congruence between nuclear and mitochondrial genes in Demospongiae: A new hypothesis for relationships within the G4 clade (Porifera: Demospongiae). Molecular Phylogenetics and Evolution, 62, 174–190. https://doi.org/10.1016/j.ympev.2011.09.016
  49. Nguyen, L.-T., Schmidt, H., von Haeseler, A. & Minh, B. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300
  50. Pankey, M.S., Plachetzki, D.C., Macartney, K.J., Gastaldi, M., Slattery, M., Gochfeld, D.J. & Lesser, M.P. (2022) Cophylogeny and convergence shape holobiont evolution in sponge-microbe symbioses. Nature Ecology and Evolution, 6, 750–762. https://doi.org/10.1038/s41559-022-01712-3
  51. de Paula, T.S., Zilberberg, C., Hajdu, E. & Lôbo-Hajdu, G. (2012) Morphology and molecules on opposite sides of the diversity gradient: Four cryptic species of the Cliona celata (Porifera, Demospongiae) complex in South America revealed by mitochondrial and nuclear markers. Molecular Phylogenetics and Evolution, 62, 529–541. https://doi.org/10.1016/j.ympev.2011.11.001
  52. Redmond, N.E., Morrow, C.C., Thacker, R.W., Diaz, M.C., Boury-Esnault, N., Cárdenas, P., Hajdu, E., Lôbo-Hajdu, G., Picton, B.E., Pomponi, S.A., Kayal, E. & Collins, A.G. (2013) Phylogeny and systematics of Demospongiae in light of new small-subunit ribosomal DNA (18S) sequences. Integrative and Comparative Biology, 53, 388–415. https://doi.org/10.1093/icb/ict078
  53. Ridley, S.O. & Dendy, A. (1886) Preliminary report on the Monaxonida collected by H.M.S. Challenger. Part I. Annals and Magazine of Natural History, Series 5, 18 (107), 325–251. https://doi.org/10.1080/00222938609459982
  54. Ristau, D.A. (1977) Shallow-water Demospongiae of North-Central California: Taxonomy and systematics, distribution, and fossilization potential. PhD. University of California, Davis, California. [unknown pagination]
  55. Ristau, D.A. (1978) Six new species of shallow-water marine demosponges from California. Proceedings of the Biological Society of Washington, 91, 569–589.
  56. Rot, C., Goldfarb, I., Ilan, M. & Huchon, D. (2006) Putative cross-kingdom horizontal gene transfer in sponge (Porifera) mitochondria. BMC Evolutionary Biology, 6, 1–11. https://doi.org/10.1186/1471-2148-6-71
  57. Schneider, C., Rasband, W. & Eliceiri, K. (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671–675. https://doi.org/10.1038/nmeth.2089
  58. Simpson, T.L. (1966) A new species of Clathriid sponge from the San Juan Archipelago. Postilla, 103, 1–7.
  59. van Soest, R., Rützler, K. & Sim, C.-J. (2016) Crooked Anthos: proposed subgeneric status of Jia (Porifera, Poecilosclerida), with descriptions of four new species. In: Schönberg, C.H.L., Fromont, J., Hooper, N.A., Sorokin, S., Zhang, W. & de Voogd, N. (Eds.), New Frontiers in Sponge Science—the 2013 Fremantle Sponge Conference. Journal of the Marine Biological Association of the United Kingdom, 96, pp. 221–235. https://doi.org/10.1017/S002531541400191X
  60. van Soest, R.W.M. (2002) Family Hymedesmiidae Topsent, 1928. In: Systema Porifera: A Guide to the Classification of Sponges. Springer, Boston, Massachusetts, pp. 575–593. https://doi.org/10.1007/978-1-4615-0747-5_62
  61. van Soest, R.W.M. & Hajdu, E. (2002) Family Mycalidae Lundbeck, 1905. In: Hooper, J.N.A. & van Soest, R.W.M. (Eds.), Systema Porifera. A guide to the classification of sponges. Kluwer Academic/Plenum Publ., New York, New York, pp. 669–690. https://doi.org/10.1007/978-1-4615-0747-5_73
  62. Trifinopoulos, J., Nguyen, L.-T., von Haeseler, A. & Minh, B. (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44, W232–W235. https://doi.org/10.1093/nar/gkw256
  63. Turner, T.L. (2021) Four new Scopalina from Southern California: the first Scopalinida (Porifera: Demospongiae) from the temperate Eastern Pacific. Zootaxa, 4970 (2), 353–371. https://doi.org/10.11646/zootaxa.4970.2.8
  64. Turner, T.L. & Pankey, M.S. (2023) The order Axinellida (Porifera: Demospongiae) in California. Zootaxa, 5230 (5), 501–539. https://doi.org/10.11646/zootaxa.5230.5.1
  65. Urban, F. (1902) Rhabdodermella nuttingi, nov.gen. et nov. spec. Zeitschrift für Wissenschaftliche Zoologie, 71, 268–275.
  66. Urban, F. (1905) Kalifornische Kalkschwämme. (Aus dem zoologischen Institute der k. k. deutschen Universität in Pi'ag.). Archiv für Naturgeschichte, 72, 33–76.
  67. Vacelet, J. & Vasseur, P. (1971) Éponges des récifs coralliens de Tuléar (Madagascar). Téthys, Supplément 1, 51–126.
  68. Valentine, J. (1966) Numerical analysis of marine molluscan ranges on extratropical northeastern Pacific shelf. Limnology and Oceanography, 11, 198–211. https://doi.org/10.4319/lo.1966.11.2.0198
  69. Wilson, K., de Rond, T., Burkhardt, I., Steele, T.S., Schäfer, R.J.B., Podell, S., Allen, E.E. & Moore, B.S. (2023) Terpene biosynthesis in marine sponge animals. Proceedings of the National Academy of Sciences, 120, e2220934120. https://doi.org/10.1073/pnas.2220934120
  70. Zacherl, D., Gaines, S.D. & Lonhart, S.I. (2003) The limits to biogeographical distributions: insights from the northward range extension of the marine snail, Kelletia kelletii (Forbes, 1852). Journal of Biogeography, 30, 913–924. https://doi.org/10.1046/j.1365-2699.2003.00899.x