Abstract
The giant barrel sponge Xestospongia muta is a dominant member of Caribbean reef ecosystems. Populations of X. muta that have been monitored annually in plots on Conch and Pickles Reefs in the Florida Keys increased by as much as 122% between 2000 and 2012, raising questions about the processes structuring these growing populations. Microsatellite markers for the closely related Pacific giant barrel sponge X. testudinaria were optimized for X. muta using individuals from Conch and Pickles Reefs (located 5.5 km apart). Further, within one plot on Conch Reef (AQS3 − 20 m depth), each individual of X. muta was mapped and genotyped to investigate fine-scale spatial genetic structuring. Significant spatial autocorrelation was detected at 2-m distance, but the dispersal distance and neighborhood size could not be determined, suggesting that recruitment extends beyond the plot. Finally, sponge samples from Conch Reef (15- and 20-m depth) and Pickles Reefs (15-m depth) were pooled into a single population for Bayesian cluster analyses. Results showed two distinct genetic clusters in the population, Clusters 1 and 2, with a near absence of Cluster 2 sponges among the largest individuals. Comparisons of the microsatellite data with mortality and recruitment data obtained from the plots revealed that the shifting genetic structure is due to disproportionate reproduction or recruitment of Cluster 2 sponges. The selective forces responsible for this genetic shift remain unclear, but it is further evidence of the dramatic changes occurring on coral reefs in the Anthropocene.
Similar content being viewed by others
References
Abdo DA, Fromont J, McDonald JI (2008) Strategies, patterns, and environmental cues for reproduction in two temperate haliclonid sponges. Aquat Biol 1:291–302
Babcock RC (1985) Growth and mortality in juvenile corals (Goniastrea, Platygyra and Acropora): the first year. In: Proc 5th Int Coral Reef Congress 4:355–360
Babcock RC (1991) Comparative demography of three species of Scleractinian corals using age- and size-dependent classifications. Ecol Monogr 61:225–244
Bell JJ, Smith D, Hannan D, Haris A, Thomas L (2014a) Isolation and characterization of twelve polymorphic microsatellite markers for Xestospongia spp. and their use for confirming species identity. Conserv Genet Resour 6:105–106
Bell JJ, Smith D, Hannan D, Haris A, Jompa J, Thomas L (2014b) Resilience to disturbance despite limited dispersal and self-recruitment in tropical barrel sponges: implications for conservation and management. PLoS ONE 9:e91635
Birenheide R, Amemiya S, Motokawa T (1993) Penetration and storage of sponge spicules in tissues and coelom of spongivorous echinoids. Mar Biol 115:677–683
Blanquer A, Uriz MJ, Caujapé-Castells J (2009) Small-scale spatial genetic structure in Scopalina lophyropoda, an encrusting sponge with philopatric larval dispersal and frequent fission and fusion events. Mar Ecol Prog Ser 380:95–102
Calderón I, Ortega N, Duran S, Becerro M, Pascual M, Turon X (2007) Finding the relevant scale: clonality and genetic structure in a marine invertebrate (Crambe crambe, Porifera). Mol Ecol 16:1799–1810
Chaves-Fonnegra A, Feldheim K, Secord J, Lopez JV (2015) Population structure and dispersal of the coral excavating sponge Cliona delitrix. Mol Ecol 24:1447–1484
Cowart JD, Henkel TP, McMurray SE, Pawlik JR (2006) Sponge orange band (SOB): a pathogenic-like condition of the giant barrel sponge, Xestospongia muta. Coral Reefs 25:513
de Bakker DM, van Duy FC, Bak RPM, Nugues MM, Nieuwland G, Meesters EH (2017) 40 Years of benthic community change on the Caribbean reefs of Curacao and Bonaire: the rise of slimy cyanobacterial mats. Coral Reefs 36:355–367
De Goeij JM, Van Oevelen D, Vermeij MJA, Osinga R, Middelburg JJ, De Goeij AFPM, Admiraal W (2013) Surviving in the marine desert: the sponge loop retains resources within coral reefs. Science 342:108–110
Deignan LK, Pawlik JR (2015) Perilous proximity: does the Janzen-Connell hypothesis explain the distribution of giant barrel sponges on a Florida coral reef? Coral Reefs 34:561–567
Diaz MC, Rutzler K (2001) Sponges: as essential component of Caribbean coral reefs. B Mar Sci 69:535–546
Dunlap M, Pawlik JR (1996) Video-monitored predation by Caribbean reef fishes on an array of mangrove and reef sponges. Mar Biol 126:117–123
Duran S, Pascual M, Estoup A, Turon X (2004) Strong population structure in the marine sponge Crambe crambe (Poecilosclerida) as revealed by microsatellite markers. Mol Ecol 13:511–522
Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Epperson BK (2005) Estimating dispersal from short distance spatial autocorrelation. Heredity 95:7–15
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Giles EC, Saenz-Agudelo P, Hussey NE, Ravasi T, Berumen ML (2015) Exploring seascape genetics and kinship in the reef sponge Stylissa carteri in the Red Sea. Ecol Evol 5:2487–2502
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Heredity 86:485–486
Hall VR, Hughes TP (1996) Reproductive strategies of modular organisms: comparative studies of reef-building corals. Ecology 77:950–963
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes I 2:618–620
Keigwin LD Jr (1978) Pliocene closing of the Isthmus of Panama, based on biostratigraphic evidence from nearby Pacific Ocean and Caribbean Sea cores. Geology 6:630–634
Leichter JJ, Shellenbarger G, Genovese SJ, Wing SR (1998) Breaking internal waves on a Florida (USA) coral reef: a plankton pump at work? Mar Ecol Prog Ser 166:83–97
Leichter JJ, Deane GB, Stokes MD (2005) Spatial and temporal variability of internal wave forcing on a Coral Reef. J Phys Oceanogr 35:1945–1962
Leichter JJ, Stokes MD, Vilchis LI, Fiechter J (2014) Regional synchrony of temperature variation and internal wave forcing along the Florida Keys reef tract. J Geophys Res Oceans 119:548–558
Loh T-L, Pawlik JR (2014) Chemical defenses and resource trade-offs structure sponge communities on Caribbean coral reefs. Proc Natl A Sci 111:4151–4156
Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotoria officialis (Rubiaceae). Am J Bot 82:1420–1425
López-Legentil S, Pawlik JR (2009) Genetic structure of the Caribbean giant barrel sponge Xestospongia muta using the I3-M11 partition of COI. Coral Reefs 28:157–165
López-Legentil S, Song B, McMurray SE, Pawlik JR (2008) Bleaching and stress in coral reef ecosystems: Hsp70 expression by the giant barrel sponge Xestospongia muta. Mol Ecol 17:1840–1850
López-Legentil S, Erwin PM, Pawlik JR, Song B (2010) Effects of sponge bleaching on ammonia oxidizing Archaea: distribution and relative expression of ammonia monooxygenase genes associated with the barrel sponge Xestospongia muta. Microb Ecol 60:561–571
McMurray SE, Blum JE, Pawlik JR (2008) Redwood of the reef: growth and age of the giant barrel sponge Xestospongia muta in the Florida Keys. Mar Biol 155:159–171
McMurray SE, Henkel TP, Pawlik JR (2010) Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida Keys. Ecology 91:560–570
McMurray SE, Finelli CM, Pawlik JR (2015) Population dynamics of giant barrel sponges on Florida coral reefs. J Exp Mar Biol Ecol 473:73–80
McMurray SE, Pawlik JR, Finelli CM (2017) Demography alters carbon flux for a dominant benthic suspension feeder. Funct Ecol. https://doi.org/10.1111/1365-2435.12908
McMurray SE, Stubler AD, Erwin PM, Finelli CM, Pawlik JR (2018) A test of the sponge-loop hypothesis for emergent Caribbean reef sponges. Mar Ecol Progr Ser. https://doi.org/10.3354/meps12466
Meylan A (1988) Spongivory in hawksbill turtles: a diet of glass. Science 239:393–395
Moran PAP (1948) The interpretation of statistical maps. J R Stat Soc B 37:243–251
Norström AV, Nyström M, Lokrantz J, Folke C (2009) Alternative states on coral reefs: beyond coral—macroalgal phase shifts. Mar Ecol Prog Ser 376:295–306
Paradis E (2010) pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26:419–420
Pawlik JR (1983) A sponge-eating worm from Bermuda: Branchiosyllis oculata (Polychaeta, Syllidae). P.S.Z.N.I. Mar Ecol 4:65–79
Pawlik JR, Burkepile DE, Vega Thurber R (2016) A vicious circle? Altered carbon and nutrient cycling may explain the low resilience of Caribbean coral reefs. Bioscience 66:470–476
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. PeerJ 6:e4343
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249. http://genepop.curtin.edu.au/index.html
Richards VP, Bernard AM, Feldheim KA, Shivji MS (2016) Patterns in population structure and dispersal in the long-lived “redwood” of the reef, the giant barrel sponge (Xestospongia muta). Coral Reefs 35:1097–1107
Riesgo A, Blasco G, Erwin PM, Pérez-Portela R, López-Legentil S (2014) Optimization of fourteen microsatellite loci in a Mediterranean demosponge subjected to population decimation, Ircinia fasciculata. Conserv Genet Resour 6:301–303
Riesgo A, Perez-Portela R, Pita L, Blasco G, Erwin PM, Lopez-Legentil S (2016) Population structure and connectivity in the Mediterranean sponge Ircinia fasciculata are affected by mass mortalities and hybridization. Heredity 117:427–439
Ritson-Williams R, Becerro MA, Paul VJ (2005) Spawning of the giant barrel sponge Xestospongia muta in Belize. Coral Reefs 24:160
Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62
Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103-106. http://genepop.curtin.edu.au/index.html
Schmidt O (1870) Grundzüge einer Spongien-Fauna des atlantischen Gebietes. Wilhelm Engelmann, Leipzig, iii–iv, 1–88, pls I–VI:44–45
Serrano X (2013) Horizontal vs. vertical connectivity in Caribbean reef corals: identifying potential sources of recruitment following disturbance. Dissertation, University of Miami
Serrano X, Baums IB, O’Reilly K, Smith TB, Jones RJ, Shearer TL, Nunes FLD, Baker AC (2014) Geographic differences in vertical connectivity in the Caribbean coral Montastraea cavernosa despite high levels of horizontal connectivity at shallow depths. Mol Ecol 23:4226–4240
Setiawan E, de Voogd NJ, Swierts T, Hooper JNA, Wörheide G, Erpenbeck D (2016a) MtDNA diversity of the Indonesian giant barrel sponge Xestospongia testudinaria (Porifera: Haplosclerida)—implications from partial cytochrome oxidase 1 sequences. J Mar Biol Assoc UK 96:323–332
Setiawan E, De Voogd NJ, Hooper JNA, Wörheide G, Erpenbeck D (2016b) Bottomless barrel-sponge species in the Indo-Pacific? Zootaxa 4136:393–396
Smith SR (1992) Patterns of coral recruitment and post-settlement mortality on Bermuda’s Reefs: comparisons to Caribbean and Pacific Reefs. Am Zool 32:663–673
Southwell MW, Weisz JB, Martens CS, Lindquist N (2008) In situ fluxes of dissolved inorganic nitrogen from the sponge community on Conch Reef, Key Largo, Florida. Limnol Oceanogr 53:986–996
Swierts T, Peijnenburg KTCA, de Leeuw C, Cleary DFR, Hörnlein C, Setiawan E, Wörheide G, Erpenbeck D, de Voogd NJ (2013) Lock, stock and two different barrels: comparing the genetic composition of morphotypes of the Indo-Pacific sponge Xestospongia testudinaria. PLoS One 8:e74396
Swierts T, Peijnenburg KTCA, de Leeuw CA, Breeuwer JAJ, Cleary DFR, de Voogd NJ (2017) Globally intertwined evolutionary history of giant barrel sponges. Coral Reefs. https://doi.org/10.1007/s00338-017-1585-6
Taboada S, Riesgo A, Blasco G, Sola J, Xavier JB, Lopez-Legentil S (2015) Development of 10 microsatellite markers for the Atlanto-Mediterranean sponge Petrosia ficiformis. Conserv Genet Resour 7:895–897
Uriz MJ, Turon X, Becerro MA, Galera J, Lozano J (1995) Patterns of resource allocation to somatic, defensive, and reproductive functions in the Mediterranean encrusting sponge Crambe crambe (Demospongiae, Poecilasclerida). Mar Ecol Prog Ser 124:159–170
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Wahab MAA, de Nys R, Webster N, Whalan S (2014) Phenology of sexual reproduction in the common coral reef sponge, Carteriospongia foliascens. Coral Reefs 33:381–394
Wahab MAA, de Nys R, Holzman R, Schneider CL, Whalan S (2017) Patterns of reproduction in two co-occurring Great Barrier Reef sponges. Mar Freshw Res 68:1233–1244
Whalan S, Battershill C, de Nys R (2007) Sexual reproduction of the brooding sponge Rhopaloeides odorabile. Coral Reefs 26:655–663
Wilson J, Harrison (2005) Post-settlement mortality and growth of newly settled reef corals in a subtropical environment. Coral Reefs 24:418–421
Wulff JL (1995) Sponge-feeding by the Caribbean starfish Oreaster reticulatus. Mar Biol 123:313–325
Zea S (1993) Cover of sponges and other sessile organisms in rocky and coral reef habitats of Santa Marta, Colombian Caribbean Sea. Caribb J Sci 29:75–88
Acknowledgements
This study was funded by grants to J.R.P. from the National Undersea Research Program at UNCW (NOAA NA96RU-0260), NOAA’s Coral Reef Conservation Program, and the National Science Foundation, Biological Oceanography Program (OCE-0095724, 0550468, 1029515, 1558580). We thank the staff of the NOAA’s Aquarius Reef Base in Key Largo, Florida, for logistical support. Research in the Florida Keys National Marine Sanctuary was performed under permit FKNMS-2009-126-A1.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable guidelines for the collection of sponge tissue samples were followed under permit FKNMS-2009-126-A1.
Data Accessibility
GenBank accession numbers KY858934 to KY858942.
Additional information
Responsible Editor: S. Uthicke.
Reviewed by M. A. Wahab and an undisclosed expert.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Deignan, L.K., Pawlik, J.R. & López-Legentil, S. Evidence for shifting genetic structure among Caribbean giant barrel sponges in the Florida Keys. Mar Biol 165, 106 (2018). https://doi.org/10.1007/s00227-018-3355-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-018-3355-6