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New epizooic symbioses between sponges of the genera Plakortis and Xestospongia in cryptic habitats of the Caribbean

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Abstract

Three new cases of sponge symbiosis between species of Plakortis and Xestospongia were found in reef caves and mesophotic reef habitats of the Caribbean. Plakortis sp. 1 from the Bahamas associates exclusively with Xestospongia deweerdtae which was originally described living freely on the deep fore-reef and caves of Jamaica. In addition, we found Plakortis sp. 2 from Puerto Rico which associates with both X. deweerdtae and a different Xestospongia sp. Sponge specimens were identified using cytochrome oxidase subunit 1, 28S rRNA and 18S rRNA gene sequence fragments, spicule analysis, and histological sections with SEM. Unlike previous sponge pairs, Xestospongia spp. not only grew as a thin veneer of tissue over the Plakortis host sponge but through the mesohyl, forming inner channels (0.1–1 cm) that may provide a benefit by facilitating more efficient water transport through the dense Plakortis tissue. Symbioses with both Plakortis spp. were documented from an early recruit stage through adulthood. Spicule measurements conducted on symbiotic versus free-living X. deweerdtae revealed significantly smaller spicule sizes for symbiotic individuals, suggesting a cost in terms of silicon availability, or a benefit in terms of a lower investment in skeleton synthesis for support. This study reveals new specialized symbiotic associations between distantly related sponge genera that likely represent an alternative strategy of adaptation for life in reef caves and mesophotic reefs.

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Acknowledgments

Funding for this project was supported by NOAA’s Living Marine Resource Cooperative Science Center award number NA11SEC4810002. JV received additional support by the American Museum of National History Lerner-Gray Fund for Marine Research for the collection of sponges in Puerto Rico. JV’s stipend was provided by NOAA’s Nancy Foster Scholarship award NA12NOS4290142. Support for sequencing of sponge samples was provided by the NSF BIO/IOS Program (IOS-0919728) Grant to RTH. We would like to thank the government of the Bahamas for letting us collect samples provided by an unnumbered scientific permit for the operation of the R/V Walton Smith in their territorial waters; the government of Mexico for providing the CONAPESCA permit DAPA/2/06504110612/1608; and the government of Puerto Rico for providing permit 2010-IC-043 (R-VS-PVS15-SJ-00190-08062010). All sponge collections from the Bahamas and Mexico were supported by NSF award OCE-1029515 to JRP. Scanning electron microscope images were provided by the University of Maryland Baltimore County’s NanoImaging facility with the assistance of Dr. Laszlo Takacs. Paul Jensen and Laura Grice are thanked for providing key points to the discussion of this manuscript. Micah Marty is thanked for his assistance in performing dissections and photographing sponge individuals during cruises to the Bahamas. JV is indebted to Milton Carlo at the University of Puerto Rico at Mayaguez for his dive assistance with the collection of sponge individuals from Puerto Rico. Fred Lentz and Jose A. Rivera are also thanked for providing boat access for the collection of sponges in Desecheo, Puerto Rico. Niamh E. Redmond is thanked for her advice in suggesting primers for this study. We thank Leah Blasiak for her assistance in troubleshooting phylogenetic tree analyses. Nilli Zmora is thanked for providing histological equipment to perform hematoxylin and eosin staining for light microscopy images. SZ’s work is contribution of the Centro de Estudios en Ciencias del Mar – CECIMAR, Universidad Nacional de Colombia, Sede Caribe. We thank two anonymous reviewers for very helpful comments. This is IMET contribution no. 14–136 and UMCES contribution no. 4960.

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Authors and Affiliations

  1. Institute of Marine and Environmental Technology, University of Maryland Center for Environmental Science, 701 E Pratt St Suite 236, Baltimore, MD, 21202, USA

    Jan Vicente, Ryan J. Powell & Russell T. Hill

  2. Centro de Estudios en Ciencias del Mar-CECIMAR, Universidad Nacional de Colombia, Sede Caribe, c/o INVEMAR, Calle 25 2-55, Rodadero Sur – Playa Salguero, Santa Marta, Colombia

    Sven Zea

  3. Department of Biology and Marine Biology, Center for Marine Science, University of North Carolina Wilmington, 5600 Marvin K. Moss Lane, Wilmington, NC, 28409, USA

    Joseph R. Pawlik

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  1. Jan Vicente
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Correspondence to Russell T. Hill.

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Communicated by M. G. Chapman.

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Supplementary material 1 (DOCX 108 kb)

227_2014_2546_MOESM2_ESM.eps

Supplementary material Phylogenetic tree generated from 1,300 bp of the 18S rRNA gene of sponges sequenced in this study (bold). Reference sequences downloaded from GenBank are indicated by species name and accession numbers. The tree topology was obtained from neighbor-joining (NJ) analysis. The bootstrap values at each node were generated from (NJ), maximum parsimony (MP), and maximum likelihood (ML) analysis, respectively (EPS 672 kb)

227_2014_2546_MOESM3_ESM.eps

Supplementary material Phylogenetic tree generated from 463 bp of the cytochrome oxidase subunit I of sponges sequenced in this study (bold). Reference sequences downloaded from GenBank are indicated by species name and accession numbers. The tree topology was obtained from neighbor-joining (NJ) analysis. The bootstrap values at each node were generated from (NJ), maximum parsimony (MP), and maximum likelihood (ML) analysis, respectively (EPS 668 kb)

227_2014_2546_MOESM4_ESM.eps

Supplementary material SEM images of (A) diods and triods from Plakortis sp. 1, (B) diods and triods from Plakortis sp. 2, (C) diods from Plakortis halichondrioides, (D) strongyles from free-living X. deweerdtae, (E) strongyles from associated X. deweerdtae, (F) isodictyal reticulation of oxeas from Xestospongia sp. Scale bar for all images 100 µm (EPS 22754 kb)

227_2014_2546_MOESM5_ESM.eps

Supplementary material Field marked specimens of Plakortis sp. 2/Xestospngia sp. (20–23) and Plakortis sp. 2/X. deweerdtae (24) monitored for growth over eight months. Scale bar for sponges photographed in August 2012 (20) 2 cm, (21) 3 cm, (22) 1 cm, (23) 2 cm, (24) 3 cm (EPS 204317 kb)

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Vicente, J., Zea, S., Powell, R.J. et al. New epizooic symbioses between sponges of the genera Plakortis and Xestospongia in cryptic habitats of the Caribbean. Mar Biol 161, 2803–2818 (2014). https://doi.org/10.1007/s00227-014-2546-z

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