Printer Friendly

Low functional redundancy in sponges as a result of differential picoplankton use.


There has been increasing interest in recent years in the relationship between functional diversity (FD) and species diversity (SD), and particularly in how a reduction in species diversity might influence ecosystem functioning (Steele, 1991; Petchey and Gaston, 2002a, b, 2006; Bremner et al., 2003; Micheli and Halpern, 2005; Bremner, 2008). There has been some debate over the most suitable way to measure FD and which species traits should be used for FD characterization (Petchey and Gaston, 2006; Bremner, 2008). However, classifications based on trophic levels or energy assimilation mechanisms (e.g., Naeem, 2002; Petchey and Gaston, 2006) may overlook important functions unrelated to these processes (Bremner et al., 2003; Bremner, 2008). Furthermore, FD classification schemes based only on trophic levels have the potential to group organisms with similar evolutionary histories or food resource requirements. However, such groupings might not be appropriate since the way that different species utilize resources within different trophic levels may vary, even between closely related species. A more inclusive approach is to include traits of individual species. rather than grouping taxonomically similar species together (Naeem, 2002; Bremner, 2008).

Benthic suspension feeders are recognized as being important components of shallow marine ecosystems, where they are capable of moving large quantities of particles from the water column to the benthos (Ribes et al., 2005; Pile and Young, 2006). These organisms, through their suspension-feeding activities, affect water clarity, productivity, and bentho-pelagic coupling, a two-way inter-linked process in which detritus, nutrients, microorganisms, and planktonic particles are moved between the benthos and the pelagic ecosystem, thereby controlling and affecting pelagic processes (Menge et al., 1997; Gili and Coma, 1998). In most rocky benthic environments a large number of different suspension feeders occur in the same habitat, but in most assessments of FD these organisms are classified within a single functional group (Bremner et al., 2003; Micheli and Halpern, 2005). At higher taxonomic levels, however, sponges, ascidians, and bivalves are thought to reduce competition for food by partitioning their food resources on the basis of different-sized particles or by filtering water from different heights above the substratum (Stuart and Klumpp, 1984).

A number of experimental studies in tropical and temperate environments have quantified the particle uptake and metabolic contribution of all types of plankton to the diets of different benthic suspension-feeding taxa, including sponges, bivalves, bryozoans, tunicates, corals, and ascid-ians (Gili and Coma, 1998; Orejas etal.. 2000; Porter etal.. 2004; Pile, 2005; Ribes et al., 2005). The main dietary components of these different groups consist of dissolved organic matter, bacteria, and phytoplankton, although the uptake efficiency and capture rates of the different types of food differ within the specific groups (Gili and Coma, 1998). For example, tropical, temperate, and deep-sea sponge species vary considerably in retention efficiencies for different prey sizes (Reiswig, 1971; Pile et al., 1996; Turon et al., 1997; Witte et al., 1997; Ribes et al., 1999). We propose that the removal of different components of the phytoplankton by species from the same phylum represents different potential contributions of these species to ecosystem functioning, since different species may have the ability to influence or control the abundance of different phyto-plankton components.

Despite sponges being grouped with other suspension feeders in previous FD assessments, several studies have clearly identified the diversity of functional roles that sponges perform and the food they consume (Gili and Coma, 1998; Wulff, 2006; Bell, 2008). Furthermore, in spite of the ecological importance of sponges, few studies have looked at differences in resource use in this group (but see Hartman, 1957; Reiswig, 1973, 1974; Thurber, 2007; Yahel et al., 2006; 2007).

In an earlier study (Perea-Blazquez et al., 2012) to estimate the total amount of food consumed by an entire sponge assemblage, we collected information on sponge feeding from the same study area and using the same species examined in the present study We have re-analyzed those data to examine any differential food resource use by sponge species that live in the same local habitat; we focused on picoplankton, which constitutes a major component of the diet of sponges. We aimed to determine if different sponge species (or groups of species) utilized different components of the available picoplankton. For this purpose, we investigated the natural diet of seven sponge species (five dem-[degrees]sponges and two calcareous sponges) that co-exist on a subtidal rocky reef on the Wellington south coast in New Zealand.

Materials and Methods

Study site

This study was conducted within the Taputeranga Marine Reserve (41[degrees]20'58.5"S, 174[degrees]45'50.8"E) on the south coast of Wellington, New Zealand. The sampling site was dominated by rocky reefs that provide habitats for diverse assemblages of benthic marine organisms, and samples were all collected within a 150-m2 area. The subtidal rocky reefs along this coast support a high diversity and abundance of sponge species that are particularly found on the sides of channels, rock walls, boulders, and overhangs, or in crevices that are common in the area (Berman and Bell, 2010).

Sampling and flow cytometry analysis

Previous surveys have described the sponge biodiversity and abundance in the study area (Berman et al., 2008; Berman and Bell, 2010), and from these data we selected seven of the most common and widespread sponge species: Dysidea sp., Haliclona sp., Plakina sp., Polymastia sp., Tethya bergyuistae (Hooper and Wiedenmayer, 1994), Leu-cetta sp., and Leucosolenia echinata (Kirk, 1893). For details of the importance of these species, see Perea-Blazquez et al. (2012). Sampling was conducted by scuba divers from November 2008 to March 2009 at a maximum depth of 10 m. This relatively long time period reflects the difficulty in sampling the very dynamic environment along this coast. Samples were collected across this time period to reduce the effects of any seasonal bias.

Three specimens of each species (at least 5 m apart) were haphazardly selected, and water was sampled in the field from each specimen, using a 5-ml sterile plastic syringe with a blunt-ended needle (0.2-mm diameter). Water was slowly drawn from the inhalant stream at a distance of ~3-5 cm from the sponge ostia and then from the exhalant water inside the oscular aperture; care was taken to avoid contact with the sponge, and one syringe was used per specimen. In L. echinata, the syringe drawing water was moved along the pinacodermal layer to ensure that the inhalant stream of the sponges was being correctly sampled. The water was drawn from a single osculum from each specimen over a period of 2 to 3 min to ensure that only the exhalant flow was sampled (based on preliminary measurements using the release of fluorescent dye to determine flow rates). The syringe method has some drawbacks, as discussed by Yahel et al. (2005); however, this method has been successfully applied in other studies looking at the diet composition of temperate sponges (Pile et al., 1996; Perea-Blazquez et al., 2010; Topcu et at., 2010). Importantly, care was taken to draw the water slowly over the period of several minutes to ensure that the exhalant water leaving the sponge was sampled, rather than being sucked from the sponge. Furthermore, the use of dye experiments ensured that the exhalant water was being sampled and was not being contaminated by ambient water.

All samples were analyzed using flow cytometry. Once back in the laboratory (located about 100 m from the sample site), water samples were transferred into sterile 1.5-ml cryovials with freshly prepared glutaraldehyde (0.1% final concentration in distilled water). Samples were frozen in liquid nitrogen and stored at--80 [degrees]C following the protocol described by Marie et al. (1999) for natural seawater samples, until the flow cytometric analysis could be performed.

Seawater samples were analyzed to quantify heterotrophic bacteria (<1 Am in size) and cyanobacteria (Pro-chlorococcus spp. typically 0.6-0.8 il.M in size and Synechococcus spp. typically 0.8-1.5 p.m in size) using a BD LSR II SORP (Special Order Research Product) cytometer equipped with five lasers (see Perea-Blazquez et al., 2010; 2012, for a detailed description of the flow cytometric method).

Data analysis

We determined the retention efficiency of picoplankton particles, which was expressed as the percentage of pico-planktonic cells removed by each species from inhalant water samples; this was calculated as 1 minus the concentration of cells in the exhalant water divided by the ambient concentration of cells. We used a two-way analysis of variance (ANOVA) to model the retention efficiency of sponges against sponge species (seven levels: Dysidea sp., Plakina sp., Polymastia sp., Leucosolenia echinata, Hali-clona sp., Tethya bergguistae, Leucetta sp.) and picoplank-ton (three levels: heterotrophic bacteria, Prochlorococcus, Synechococcus). Since retention efficiency was expressed as a percentage, we square-root-transformed the data to meet assumptions of normality and equal variance. We examined the assumption of homogeneity of variances using Baitlea's test (P > 0.05 in all cases). These statistical analyses were performed by R ver. 2.10 (R Development Core Team, 2012).

Using data on the percentage retention of the three pico-plankton types, we then quantified similarity in the diet composition of the seven sponge species by using the Bray-Curtis dissimilarity index (Bray and Curtis, 1957). From the resulting dissimilarity matrix, we constructed a dendrogram to visually display (in two dimensions) sponge species relationships, where species with more similar diet compositions were more closely grouped. An ordination was then carried out using non-metric multi-dimensional scaling (nMDS) to further examine the relationships between the diet composition of the species. This ordination was based on a resemblance matrix calculated using the Bray-Curtis similarity index, and data were not transformed. ANOSIM (analysis of similarities) was then used to determine if the groups identified from the Bray-Curtis analysis and nMDS (which were consistent) were supported. Where ANOSIM R = 1, the groups are completely different and where ANOSIM R = 0, they are exactly the same. We used the Vegan package to calculate the Bray-Curtis dissimilarity matrix and construct dendrograms, and PRIMER (ver. 6) to construct the nMDS plot and conduct the ANOSIM analysis.


Picoplankton removal

We identified three types of picoplanktonic organisms (heterotrophic bacteria--HetBact; Prochlorococcus--Prochlo; and Synechococcus--Synecho) that sponges removed from the ambient (inhalant) water. The overall average ambient cell concentration of heterotrophic bacteria was markedly higher (6.0 -[+ or -] 2.4 X [10.sup.5] cells/m1) than that of Prochloro-coccus (7.2 _[+ or -] 5.2 X [10.sup.4] cells/m1) and Synechococcus (2.1 [+ or -] 1.4 X 104 cells/m1) for all samples taken from the inhalant water surrounding sponges. The retention efficiencies of the different picoplanktonic organisms varied considerably between the sponge species. There was a significant interaction in the retention efficiency between species and types of picoplankton (ANOVA [F.sub.12,42.] = 15.934, P < 0.001). All species removed Prochlorococcus cells with the highest efficiency (range 53% to 94%), except for Leuco-solenia echinata, which removed Synechococcus cells with the highest efficiency (71%). The retention efficiencies of heterotrophic bacteria and Synechococcus cells varied considerably between many of the species; heterotrophic bacterial cells were generally retained with the lowest efficiency (about 40%, five of seven sponge species; Fig. 1).


                         HetBact    Prochlo    Synecho

Dysidea sp.              A                1    *

Haliclona sp.            B                2    +

Leucetta sp.             C                1    *

Leucosolenia echinata    A                1    *

Plakina sp.              A                1    *

Ploymastia sp.           A                1    *

Tethya bergquistae       D                2    *

Figure 1. Retention efficiency expressed as the percentage
of heterotrophic bacteria (HetBact). Prochloro-coccus
(Prochlo), and Synechococcus (Synecho) cells removed by
seven sponge species (n = 3). Bars indicate standard
deviation. Species that had retention efficiencies that
were not significantly different for each pico-plankton
type are indicated by same number (HetBact). letter
(Prochlo), or symbol (Synecho).

Note: Table made from bar graph.

Food resource utilization

Both the Bray-Curtis analysis and nMDS identified three groups of sponge species that retained similar amounts of the different picoplanktonic organisms (dissimilarity range 0.022-0.33; Fig. 2): (I) Dysidea sp., Plakina sp., Polymastia sp., and Leucosolenia echinata; (II) Haliclona sp. and Tethya bergquistae; (III) Leucetta sp. Species in group I had moderate retention rates of Prochlorococcus cells (53%71%) and Synechococcus cells (52%-67%), and a low retention rate of heterotrophic bacteria (24%-33%), while Leucosoloenia echinata was the only species that retained Synechococcus cells with a high efficiency (71%). Species in group II had high retention of Prochlorococcus cells (88%-94%) and heterotrophic bacteria (73%-90%), and removed a lower percentage of Synechococcus cells (32%52%) than did sponges in group I. Leucetta sp. (group III) did not group with any of the other species and removed considerably more Synechococcus (46%) and F'rochloro-coccus cells (58%) than heterotrophic bacteria; it was the only species that had a very low retention efficiency of heterotrophic bacteria (4%, Fig. 1). ANOSIM values were all close to 1, providing strong support for the three groups: 0.83 (groups I and III), 0.93 (groups II and III), and 0.98 (groups I and II).


Functional diversity is important when trying to understand ecosystem functioning. Although previous research suggests high levels .of functional redundancy in marine systems (Bremner et a/., 2003; Michelli and Halpern, 2005), our results suggest that sponges should not be considered as a single functional or trophic group since different groups of species appear to specialize on different food particles. Our results demonstrated that most sponges are highly efficient at retaining cyanobacteria and heterotrophic bacterial cells, but that groups of species retain the different fractions with differing efficiencies, suggesting differential picoplankton resource use. Finally, the patterns we report provide some evidence for niche partitioning in sponges, although that aspect was not specifically investigated here.

Intra-phyletic fitnctional diversity

A consistent trend among studies of functional diversity has been to classify suspension feeders into a single functional group (Bremner et al., 2003; Petchey and Gaston, 2006), even though such groupings may encompass multiple phyla. For sponges (and likely other phyla), the functional roles they fulfill are diverse and well-known (Bell, 2008). However, even within such detailed functional assessments of sponges, suspension feeding has been considered a single functional role (e.g., Bell, 2007), yet our results suggest that different sponge species have the ability to influence different components of the phytoplanktonic community. This demonstrates that suspension feeders should not be defined as a single group within functional diversity assessments, even with respect to individual phyla. There has been an increasing trend to base functional assessments on trait analysis (Bremner, 2008: Papageorgiou et at., 2009), but what is evident from these studies is the data deficiency for most species, which severely inhibits our ability to assess functional diversity.

Mechanisms of food partitioning

Although we did not investigate the mechanisms by which different groups of sponges are able to retain different proportions of the picoplankton fractions or the reasons for which they do so, several possibilities exist. These include size (Stuart and Klumpp, 1984; Ribes et al., 1999), aquiferous architecture (Leys and Eerkes-Medrano, 2006), food concentration in the surrounding water (Duckworth et al., 2003), the physiological condition of the sponges (Osinga et al., 2001), or perhaps the nutritional value of the food sources since the different components of the pico-plankton contain different amounts of carbon. The mechanism for use of these differential food resources should be the focus of future investigations.


A. Perea-Blazquez is grateful to Victoria University of Wellington for providing funding and a Ph.D. scholarship. We acknowledge Dr. M. Kelly and J. Berman for their taxonomic assistance. We are also grateful to K. Price for her help with the flow cytometry analyses and to B. Magafia-Rodriguez for statistical advice. We thank B. Magafia-Rodriguez, J. Berman. and D. Dlaz-Guisado for their assistance in the field. The Department of Conservation is also acknowledged for permitting field work within the Taputeranga Marine Reserve (permit docDM-336985).

Literature Cited

Bell, J. J. 2007. Contrasting patterns of species and functional composition of coral reef sponge assemblages. Mar. awl. Prog. Ser. 339: 73-81.

Bell., J. J. 2008. The functional roles of marine sponges. Estuar. Coast. Shelf Sci. 79: 341-353.

Berman, J., and J. J. Bell. 2010. Spatial variability of sponge assemblages on the Wellington South Coast, New Zealand. Open Mar. Biol. .1. 4: 12-25.

Berman, J., A. Perea-Blazquez, M. Kelly, and J. J. Bell. 2008. Sponges of the Wellington south coast. Pp. 225-236 in The Taput-eranga Marine Reserve, I ed., J. Gardner and J. Bell. eds. First Edition Ltd., Wellington, New Zealand.

Bray, J. R., and J. T. Curtis. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27: 325-349.

Bremner, J. 2008. Species' traits and ecological functioning in marine conservation and management. J. Exp. Mar. Biol. Ecol, 366: 37-47.

Bremner, J., S. I. Rogers, and C. L. J. Frid. 2003. Assessing functional diversity in marine benthic ecosystems: a comparison of approaches. Mar. Ecol. Prog. Ser. 254: 11-25.

Duckworth, A. R., G. A. Samples, A. E. Wright, and S .A. Pomponi. 2003. In vitro culture of the tropical sponge Axinella corrugata (Demospongiae): effect of food cell concentration on growth, clearance rate, and biosynthesis of stevensine. Mar. Biotechnol. 5: 519-527.

Gili, J. M., and R. Coma. 1998. Benthic suspension feeders: their paramount role in littoral marine food webs. Trend. Ecol. Eval. 13: 316-321.

Hartman, W. D. 1957. Ecological niche differentiation in the boring sponges (Clioniclae). Evolution 11: 294-297.

Leys, S. P., and D. I. Eerkes-Medrano. 2006. Feeding in a calcareous sponge: particle uptake by pseudopodia. Biol. Bull. 211: 157-171.

Marie, D., C. P. D. Brussaard, R. Thyrhaug, G. Bratbak, and D. Vaulot. 1999. Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl. Environ. Mierobiol. 65: 45-52.

Menge, B. A., B. A. Daley, P. A. Wheeler, E. Dahlhoff, E. Sanford, and P. T. Strub. 1997. Benthic-pelagic links and rocky intertidal communities: bottom-up effects on top-down control? Proc. Natl. Acad. Sci. 94: 14530-14535.

Micheli, F., and B. S. Halpern. 2005. Low functional redundancy in coastal marine assemblages. Ecol. Lett. 8: 391-400.

Naeem, S. 2002. Autotrophic-heterotrophic interactions and their impacts on biodiversity and ecosystem functioning. Pp. 96-119 in Functional Consequences of Biodiversity, A. Kinzig, S. Pacala, and D. Tilman. eds. Princeton University Press, Princeton. NJ.

Orejas, C., J. M. Gill, W. E. Arntz, J. D. Ros, P. J. Lopez, N. Teixido, and P. Filipe. 2000. Benthic suspension feeders, key players in Antarctic marine ecosystems? Contrib. Sci. 1: 299-311.

Osinga, R., R. Kicking E. Groenendijk, P. Niesink, J. Tramper, and R. H. Wijffels. 2001. Development of in vivo sponge cultures: particle feeding by the tropical sponge Pseudosuberites aft. andrewsi. Mar. Biotechnol. 3: 544-554.

Papageorgiou, N., K. Sigala. and I. Karakassis. 2009. Changes of macrofaunal functional composition at sedimentary habitats in the vicinity of fish farms. Estuar. Coast. Shelf Sci. 83: 561-568. doi: 10.1016/j.ecss.2009.05.002

Perea-Blazquez, A., K. Price, S. K. Davy, and J. J. Bell. 2010. Diet composition of two temperate calcareous sponges: Leucosolenia echi-nata and Leucetta sp. from the Wellington South Coast, New Zealand. Open Mar. Biol. J. 4: 65-73.

Perea-Bhizquez, A., S. K. Davy, and J. J. Bell. 2012. Estimates of particulate organic carbon flowing from the pelagic environment to the benthos through sponge assemblages. PLUS ONE 7(1): e29569. doi: 1 0.1371/journal.pone.0029569

Petchey, O. L., and K. J. Gaston. 2002a. Extinction and the loss of functional diversity. Proc. R. Soc. Biol. Sci. 269: 1721-1727.

Petchey, O. L., and K. J. Gaston. 2002b. Functional diversity (FD), species richness and community composition. Ecol. Lett. 5: 402-411.

Petchey, O. L., and K. J. Gaston. 2006. Functional diversity: back to basics and looking forward. Ecol. Lett. 9: 741-758.

Pile, A. J. 2005. Overlap in diet between co-occurring active suspension feeders on tropical and temperate reefs. Bull. Mar. Sci. 76: 743-749.

Pile, A. J., and C. M. Young. 2006. The natural diet of a hexactinellid sponge: benthic-pelagic coupling in a deep-sea microbial food web. Deep-Sea Res. 153: 1148-1156.

Pile, A. J., M. R. Patterson, and J. D. Witman. 1996. In situ grazing on plankton <10 [micro]m by the boreal sponge Mycale lingua. Mar. Ecol. Prog. Ser. 141: 95-102.

Porter, E. T., J. C. Cornwell, and L. P. Sanford. 2004. Effect of oysters Crassostrea virginica and bottom shear velocity on benthicpelagic coupling and estuarine water quality. Man Ecol. Prog. Ser. 271: 61-75.

R Development Core Team. 2012. R: A Language and Environment for Statistical Computing. Vienna, Austria. ISBN-3-900051-07-0.

Reiswig, H. M. 1971. Particle feeding in natural populations of three marine demosponges. Biol. Bull. 141: 568-591.

Reiswig, H. M. 1973. Population dynamics of three Jamaican Demo-spongiae. Bull. Mar. Sci. 23: 191-226.

Reiswig, H. M. 1974. Water transport. respiration and energetics of three tropical marine sponges. J. Exp. Mar. Biol. Ecol. 14: 231-249.

Ribes, M., R. Coma, and J. M. Gill. 1999. Natural diet and grazing rate of the temperate sponge Dysidea avarct (Demospongiae, Dendrocer-atida) throughout an annual cycle. Mar. Ecol. Prog. Ser. 176: 179-190.

Ribes, M., R. Coma, M. J. Atkinson, and R. A. Kinzie. 2005. Sponges and ascidians control removal of particulate organic nitrogen from coral reef water. LitnnoL Oceanogr. 50: 1480-1489.

Steele, J. H. 1991. Marine functional diversity. Bioscience 41: 470-474.

Stuart, V., and D. W. Kiumpp. 1984. Evidence for food-resource partitioning by kelp-bed filter feeders. Mar. Ecol. Pros. Set-. 16: 27-37.

Thurber, A. R. 2007. Diets of Antarctic sponges: links between the pelagic microbial loop and benthic metazoan food web. Mar. Ecol. Prog. Ser. 351: 77-89.

Topcu, N. E., T. Perez, G. Gregori, and M. Harrnelin-Vivien. 2010. In situ investigation of Spongia officinalis (Demospongiae) particle feeding: coupling flow cytometry and stable isotope analysis. J. Exp. Mar. Biol. Ecol. 389: 61-69.

Turon, X., J. Galera, and M. J. Uriz. 1997. Clearance rates and aquiferous systems in two sponges with contrasting life-history strategies. J. Exp. Zool. 278: 22-36.

Witte, U., T. Brattegard, G. Graf., and B. Springer. 1997. Particle capture and deposition by deep sea sponges from the Norwegian-Greenland Sea. Mar. Ecol. Prog. Ser. 154: 241-252.

Wulff, J. L. 2006. Ecological interactions of marine sponges. Can. J. Zool. 84: 146-166.

Yahel, G.. D. Marie, and A. Genin. 2005. lnEx-a direct in situ method to measure filtration rates, nutrition, and metabolism of active suspension feeders. LitnnoL Oceattogr. 3: 46-58.

Yahel, G., D. I. Eerkes-Medrano, and S. P. Leys. 2006. Size independent selective filtration of ultraplankton by hexactinellid glass sponges. Aquat. Microb. Ecol. 45: 181-194.

Yahel, G., F. Whitney, H. M. Reiswig, D. I. Eerkes-Medrano. and S. P. Leys. 2007. In situ feeding and metabolism of glass sponges (Hexactinellida. Porifera) studied in a deep temperate fjord with a remotely operated submersible. Linznol. Oceanogr. 52: 428-440.


School of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington, New Zealand

Received 26 April 2012; accepted 8 January 2013.

* To whom correspondence should be addressed. E-mail:
COPYRIGHT 2013 University of Chicago Press
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2013 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Perea-Blazquez, Alejandra; Davy, Simon K.; Bell, James J.
Publication:The Biological Bulletin
Article Type:Report
Geographic Code:8NEWZ
Date:Feb 1, 2013
Previous Article:Ferulic acid: a natural antioxidant against oxidative stress induced by oligomeric A-beta on sea urchin embryo.
Next Article:Color pattern variation in a shallow-water species of opisthobranch mollusc.

Terms of use | Privacy policy | Copyright © 2022 Farlex, Inc. | Feedback | For webmasters |