A love letter to sponges

Aplysina fistularis. Photo courtesy of ryanphotographic.com

Aplysina fistularis. Photo courtesy of ryanphotographic.com

Like many kids interested in marine biology, growing up I wanted to work on sharks. After college I interned for a year at the Center for Shark Research at the Mote Marine Lab under the guidance of two great mentors, Jim Gelsleichter and Michelle Heupel. After my internship I started my Master’s degree with Mahmood Shivji, whose research focuses broadly on conservation genetics of sharks and billfish, but who had recently received funding from the National Coral Reef Institute. Mahmood asked me how felt about working on marine invertebrates instead of sharks and since I’m a go with the flow person (much like a sponge), I said, sure, why not? That was ten years ago and I’ve never looked back.

Sponges (phylum Porifera) have a global distribution and are found in both fresh and saltwater from polar seas to tropical coral reefs. There are over 8,000 valid species with an estimated 4,000 left to be described. Sponges are sessile as adults and disperse through a mobile larvae phase. Some sponge species are hermaphroditic and some have separate sexes. Many species have internal fertilization and brood their larvae to an advanced developmental stage while other species broadcast spawn their gametes and fertilization takes in the water column. Sponges come in a range of shapes, colors, textures, and sizes. In this post, I highlight some of the amazing research conducted on sponges focusing on topics related to molecular ecology, phylogenetics, and evolution, with some other fun facts thrown in.

1. They are masters at what they do

Although they look like they are sitting around the reef like bumps on a log, sponges are continuously filter feeding by pumping massive quantities of water through their bodies (click here to see a sponge in action). The azure vase sponge, Callyspongia plicifera, pumps 6.5 liters of water per second per kilogram of dry sponge weight (Weisz et al. 2008)! Sponges strain out bacteria, viruses, and other microscopic particles, leaving the water exiting the top of the sponge tube (the osculum) virtually sterile. By pumping all this water, sponges recycle dissolved organic matter and make it available for higher trophic levels (for more on this topic see #7).

2. They are ancient

Phylogenomic estimates suggest the last common ancestor of sponges and the eumetazoans (the Ctenophora, Cnidaria, and Bilateria, but see #5) existed in the Cryogenian some 700 million years ago and sponge fossils date to the Cambrian 500 mya. Recently, Yin et al. published findings of a 600 million year old fossil preserved at the cellular level dating from the Pre-Cambrian. The fossil contains many Poriferan features such as cells resembling sponge pinocytes and a hollow tubular structure that suggests a body plan for pumping water. Although based on a single specimen, the finding points to the existence of sponges predating the Cambrian.

Individual sponge can also live to be ancient. Xestospongia muta, the giant barrel sponge, is considered the redwood of the reef (see image below). Research from the Pawlik Lab at UNC Wilmington suggests large X. muta sponges in the Florida Keys may be as old as 2000 years, making them among the oldest organisms on earth (McMurray et al. 2008).

A diver inside a giant barrel sponge. Photo from deepseanews.com

A diver inside a giant barrel sponge. Photo from deepseanews.com

3. They’re more sophisticated than you think

As early metazoans, sponges are excellent models of animal development and complexity. Although they lack conventional muscles and a nervous system, they are capable of complex and coordinated movements or behaviors in response to their environment. Ludeman et al. 2014 demonstrated that the cilia in sponge oscula serve a sensory function and are involved in the coordination of simple behaviors. For example, in the video found here, you can see a sponge contract, or “sneeze” in an effort to expel sediments clogging its filtration system.

Examining sponge complexity from a genomic perspective, Riesgo et al. 2014 collected transcriptome data from species across all four sponge classes. They found all classes shared a large complement of genes with other metazoans and three classes (calcareous, hexactinellid, and homoscleromorph sponges) shared more genes with bilaterians than with nonbilateran metazoans.

4. Their shapes can be deceiving

Traditional sponge taxonomy focused on the presence, absence, and morphology of spicules, macro- and microscopic calcareous and siliceous structures within the sponge tissue (see image below), and the overall shape, color, and texture of the sponge. However, spicule morphology and sponge shape can be influenced by biotic and abiotic factors such as water chemistry (Maldonado et al. 2012), wave action (Palumbi 1986, Bell et al. 2002), and predation (Loh & Pawlik 2009, Hill & Hill 2002). Not surprisingly, morphology and molecular species boundaries often conflict. Cryptic species, where conserved morphology conceals deep evolutionary splits, are prevalent in the Porifera (Blanquer & Uriz 2007, Xavier et al. 2010, de Paula et al. 2012) and in my own work I found that four species described based on growth form (tube, rope, and massive shapes) belonged to the same evolutionary lineage. Variation in spicule morphology in these taxa was partitioned by geography, not current species boundaries (DeBiasse & Hellberg 2015). Splitting based on misleading morphology has been documented in other sponge species as well (Xavier et al. 2010, Escobar et al. 2012, de Paula et al. 2012, Loh et al. 2012).

Sponge spicule diversity. From van Soest et al. (2012)

Sponge spicule diversity. From van Soest et al. (2012)

5. They are a phylogenetic mess… but we’re figuring it out

Early molecular phylogenetic analyses in sponges have revealed paraphyly at many taxonomic levels. In fact, some phylogenies have questioned whether the phylum is monophyletic (Sperling et al. 2007, Nosenko et al. 2013). The position of sponges in the grand tree of life is also controversial. Recent studies have shuffled the positions of the Porifera, Placozoa, Ctenophora, Cnidaria, and Bilateria (Dunn et al. 2008, Phillipe et al. 2009, Nosenko et al. 2013, Ryan et al. 2013). A consortium of labs has been working for the last several years to assemble the Porifera Tree of Life and although many questions remain, our understanding of the phylogenetic relationships within the Porifera has improved dramatically. The Porifera TOL team held a symposium at the 2013 Annual Meeting of the Society for Integrative and Comparative Biology (SICB) and papers from the conference were published in the September 2013 issue of Integrative and Comparative Biology.

6. Some sponges are coral killers…..

A species interaction that plays a large role in shaping the physical and community structure on coral reefs is the one between stony corals and bioeroding sponges, particularly those in the genus Cliona. Corals are reef builders that create the complex physical structure required for healthy coral reef ecosystem function. Clionaid sponges play an opposing role on coral reefs by bioeroding calcium carbonate substrata such as coral skeletons, thereby facilitating calcium carbonate cycling through the system. On healthy reefs, bioerosion and accretion rates are approximately equal. However, bioeroding sponges are increasing in abundance and their effects on coral reefs are leading to long-term changes in community structure and physical stability. Furthermore, evidence suggests climate change conditions stressful to corals, such as elevated temperature and decreased pH, may promote excavation in Cliona sponges. For example, Stubler et al. 2014 found  increased bioerosion rates in C. varians and decreased calcification in Porites furcata corals exposed to lowered pH conditions predicted for the year 2100 (see figure below). Wisshak et al. 2012 found a similar increase in bioerosion in an Australian Cliona species, C. orientalis. For excellent perspective on how coral reefs may shift to sponge dominated systems, see Bell et al. 2013.

 

 

Macro- and SeM images of Porites furcata specimens from ambient, moderate and high pCO2 treatments. a, b, c P. furcata fragment used in subsequent SeM imaging from each of the three pCO2 treatment levels; arrows indicate regions of Cliona varians attachment and erosion. SeM images (d, e, f) are of P. furcata skel- etal regions that were free of C. varians infestation throughout the entirety of the experiment. g, h, i SeM images of C. varians attach- ment sites and sponge erosional scars on P. furcata from each pCO2 level, as previously indicated by arrows in a, b, c (sponge removed for imaging purpose). Scale bars from all SeM images d, e, f, g, h, i) are 250 μm

Macro- and SEM images of Porites furcata specimens from ambient, moderate and high pCO2 treatments. a, b, c P. furcata fragment used in subsequent SEM imaging from each of the three pCO2 treatment levels; arrows indicate regions of Cliona varians attachment and erosion. SEM images (d, e, f) are of P. furcata skeletal regions that were free of C. varians infestation throughout the entirety of the experiment. g, h, i SEM images of C. varians attachment sites and sponge erosional scars on P. furcata from each pCO2 level, as previously indicated by arrows in a, b, c (sponge removed for imaging purpose). Scale bars from all SEM images d, e, f, g, h, i) are 250 μm. Figure and caption from Stubler et al. 2014

7. …but they make the persistence of coral reefs possible

Darwin’s paradox asks how coral reefs, one of the most species rich and productive ecosystems on earth, can persist in a nutrient poor marine desert. In 2013 de Goeij et al. used food web experiments and stable isotopes to show sponges make dissolved organic matter (DOM) available to higher trophic levels by continuously shedding filter cells that can be consumed by reef fauna.

8. They have cool patterns of population structure

Duran and Rützler 2006 showed genetic variation in Chondrilla caribensis was partitioned according to habitat type, not geography. Sponges sampled from mangroves in Belize, Florida, and Panama were genetically more similar to sponges from other mangrove locations than they were to geographically adjacent C. caribensis on coral reefs, suggestive of local adaptation and ecological speciation. More recently, Chaves-Fonegra et al. showed populations of Cliona deletrix (see image below) in Florida are separated by depth, not geographic distance.

Bright orange Cliona deletrix encrusting a stony coral. Photo courtesy of The Sponge Guide www.spongeguide.org

Bright orange Cliona deletrix encrusting a stony coral. Photo courtesy of The Sponge Guide www.spongeguide.org

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

The research I have presented here is a tiny snapshot of the incredible work being conducted on sponges by researchers worldwide. Sponges may not be as popular as sharks, but I hope I have convinced you of their ecological and evolutionary importance and perhaps inspired you to learn more about these awesome animals.

References

#1

Weisz, J. B., Lindquist, N., & Martens, C. S. (2008). Do associated microbial abundances impact marine demosponge pumping rates and tissue densities? Oecologia155 (2), 367-376. DOI: 10.1007/s00442-007-0910-0

#2

Yin, Z., Zhu, M., Davidson, E. H., Bottjer, D. J., Zhao, F., & Tafforeau, P. (2015). Sponge grade body fossil with cellular resolution dating 60 Myr before the Cambrian. Proceedings of the National Academy of Sciences, in press. DOI: 10.1073/pnas.1414577112

McMurray, S. E., Blum, J. E., & Pawlik, J. R. (2008). Redwood of the reef: growth and age of the giant barrel sponge Xestospongia muta in the Florida Keys. Marine Biology155 (2), 159-171. DOI: 10.1007/s00227-008-1014-z

#3

van Soest, R. W., Boury-Esnault, N., Vacelet, J., Dohrmann, M., Erpenbeck, D., De Voogd, N. J., … & Hooper, J. N. (2012). Global diversity of sponges (Porifera). PLoS One(4), e35105. DOI: 10.1371/journal.pone.0035105

Maldonado, M., H. Cao, X. Cao, et al. 2012. Experimental silicon demand by the sponge Hymeniacidon perlevis reveals chronic limitation in field populations. Hydrobiologia 687:251–257. DOI: 10.1007/s10750-011-0977-9

Palumbi, S. R. 1986. How body plans limit acclimation: responses of a demosponge to wave force. Ecology 67:208–214. www.jstor.org/stable/1938520

Bell, J. J., D. Barnes, and J. Turner. 2002. The importance of micro and macro morphological variation in the adaptation of a sublittoral demosponge to current extremes. Mar. Biol. 140:75–81. DOI: 10.1007/s002270100665

Loh, T.-L., and J. R. Pawlik. 2009. Bitten down to size: fish predation determines growth form of the Caribbean coral reef sponge Mycale laevis. J. Exp. Mar. Biol. Ecol. 374:45–50. DOI: 10.1016/j.jembe.2009.04.007

Hill, M. S., and A. L. Hill. 2002. Morphological plasticity in the tropical sponge Anthosigmella varians: responses to predators and wave energy. Biol. Bull. 202:86-95.  www.biolbull.org/content/202/1/86.short

Blanquer, A., and M. Uriz. 2007. Cryptic speciation in marine sponges evidenced by mitochondrial and nuclear genes: a phylogenetic approach. Mol. Phylogenet. Evol. 45:392–397. DOI: 10.1016/j.ympev.2007.03.004

Xavier, J., P. Rachello-Dolmen, F. Parra-Velandia, et al. 2010. Molecular evidence of cryptic speciation in the “cosmopolitan”, excavating sponge Cliona celata (Porifera, Clionaidae). Mol. Phylogenet. Evol. 56:13–20. DOI: 10.1016/j.ympev.2010.03.030

de Paula, T. S., C. Zilberberg, E. Hajdu, and G. Lobo-Hajdu. 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. Mol. Phylogenet. Evol. 62:529–541. DOI: 10.1016/j.ympev.2011.11.001

DeBiasse, M. B., & Hellberg, M. E. (2015). Discordance between morphological and molecular species boundaries among Caribbean species of the reef sponge CallyspongiaEcology and Evolution, 5 (3), 663-675. DOI: 10.1002/ece3.1381

Escobar, D., S. Zea, and J. A. Sanchez. 2012. Phylogenetic relationships among the Caribbean members of the Cliona viridis complex (Porifera, Demospongiae, Hadromerida) using nuclear and mitochondrial DNA sequences. Mol. Phylogenet. Evol. 64:271–284. DOI: 10.1016/j.ympev.2012.03.021

Loh, T.-L., S. Lopez-Legentil, B. Song, and J. R. Pawlik. 2012. Phenotypic variability in the Caribbean orange icing sponge Mycale laevis (Demospongiae: Poecilosclerida). Hydrobiologia 687:205–217. DOI: 10.1007/s10750-011-0806-1

#4

Ludeman, D. A., Farrar, N., Riesgo, A., Paps, J., & Leys, S. P. (2014). Evolutionary origins of sensation in metazoans: functional evidence for a new sensory organ in sponges. BMC Evolutionary Biology, 14 (1), 3. DOI: 10.1186/1471-2148-14-3

Riesgo, A., Farrar, N., Windsor, P. J., Giribet, G., & Leys, S. P. (2014). The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges. Molecular Biology and Evolution, 31 (5):1102–1120. DOI: 10.1093/molbev/msu057

#5

Sperling, E. A., Pisani, D., & Peterson, K. J. (2007). Poriferan paraphyly and its implications for Precambrian palaeobiology. Geological Society, London, Special Publications, 286 (1), 355-368. DOI: 10.1144/SP286.25

Nosenko, T., Schreiber, F., Adamska, M., Adamski, M., Eitel, M., Hammel, J., … & Wörheide, G. (2013). Deep metazoan phylogeny: when different genes tell different stories. Molecular Phylogenetics and Evolution67 (1), 223-233. DOI: 10.1016/j.ympev.2013.01.010

Dunn, C.W., Hejnol, A., Matus, D.Q., Pang, K., Browne, W.E., Smith, S.A., Seaver, E., Rouse, G.W., Obst, M., Edgecombe, G.D., et al., 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745–749. DOI: 10.1038/nature06614

Philippe, H., Derelle, R., Lopez, P., Pick, K., Borchiellini, C., Boury-Esnault, N., Vacelet, J., Renard, E., Houliston, E., Queinnec, E., et al., 2009. Phylogenomics revives traditional views on deep animal relationships. Current Biology 19, 706–712. DOI: 10.1016/j.cub.2009.02.052

Ryan, J. F., Pang, K., Schnitzler, C. E., Nguyen, A. D., Moreland, R. T., Simmons, D. K., … & Baxevanis, A. D. (2013). The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science342 (6164), 1242592. DOI:10.1126/science.1242592

#6

Stubler, A. D., Furman, B. T., & Peterson, B. J. (2014). Effects of pCO2 on the interaction between an excavating sponge, Cliona varians, and a hermatypic coral, Porites furcataMarine Biology161 (8), 1851-1859. DOI: 10.1007/s00227-014-2466-y

Wisshak, M., Schönberg, C. H., Form, A., & Freiwald, A. (2012). Ocean acidification accelerates reef bioerosion. PLoS One(9), e45124. DOI: 10.1371/journal.pone.0045124

Bell, J. J., Davy, S. K., Jones, T., Taylor, M. W., & Webster, N. S. (2013). Could some coral reefs become sponge reefs as our climate changes? Global Change Biology19 (9), 2613-2624. DOI: 10.1111/gcb.12212

#7

de Goeij, J. M., van Oevelen, D., Vermeij, M. J., Osinga, R., Middelburg, J. J., de Goeij, A. F., & Admiraal, W. (2013). Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science342 (6154), 108-110. DOI: 10.1126/science.1241981

#8

Duran, S., & Rützler, K. (2006). Ecological speciation in a Caribbean marine sponge. Molecular Phylogenetics and Evolution40 (1), 292-297. DOI: 10.1016/j.ympev.2006.02.018

Chaves‐Fonnegra, A., Feldheim, K., Secord, J., & Lopez, J. V. (2015). Population structure and dispersal of the coral excavating sponge Cliona delitrixMolecular Ecology, in press. DOI: 10.1111/mec.13134

 

Share

About Melissa DeBiasse

I am a postdoctoral researcher at the University of Florida Whitney Laboratory for Marine Bioscience. As an evolutionary ecologist I am interested in the processes that generate biodiversity in marine ecosystems. My research uses experimental methods and genomic and phenotypic data to test how marine invertebrate species respond to biotic and abiotic stressors over ecological and evolutionary timescales.
This entry was posted in Uncategorized. Bookmark the permalink.