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The Society for Integrative and Comparative Biology
Impacts of Shading on Sponge-Cyanobacteria Symbioses: A Comparison between Host-Specific and Generalist Associations1
1 Department of Biology, University of Alabama at Birmingham, Birmingham, Alabama 35294-1170
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 SYNOPSIS INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The marine sponge Lamellodysidea chlorea contains large populations of the host-specific, filamentous cyanobacterium Oscillatoria spongeliae. Other marine sponges, including Xestospongia exigua, contain the generalist, unicellular cyanobacterium Synechococcus spongiarum. The impact of cyanobacterial photosynthesis on host sponges was manipulated by shading these sponge-cyanobacteria associations. If cyanobacteria benefit their hosts, shading should reduce this benefit. Chlorophyll a concentrations were measured as an index of cyanobacterial abundance. After two weeks, shaded L. chlorea lost more mass than controls, while shaded and control X. exigua did not lose a significant amount of mass. Chlorophyll a concentrations in shaded X. exigua were lower than in controls, but were not significantly different between shaded and control L. chlorea. In addition, L. chlorea shaded in situ lost over 40% of their initial area, but did not differ in chlorophyll a concentrations from controls. These results suggest that Oscillatoria symbionts benefit their host sponges in a mutualistic association. Synechococcus symbionts may be commensals that exploit the resources provided by their sponge hosts without significantly affecting sponge mass. When shaded, Synechococcus symbionts may be consumed by their hosts or may be able to disperse from this unfavorable environment. These data support the hypothesis that more specialized symbionts provide a greater benefit to their hosts, but hypotheses concerning the dispersal abilities of these symbionts remain to be explored. Sponge-cyanobacteria symbioses provide model systems for investigating the costs and benefits of symbiosis and the roles of dispersal, environmental conditions, and phylogenetic history in determining the specificity of endosymbionts for their hosts.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Symbioses between prokaryotes and metazoans are ubiquitous in marine, freshwater, and terrestrial environments. Although many of these symbioses are assumed to represent coevolved, mutually beneficial interactions, the ecological and evolutionary nature of many symbioses remain to be explored experimentally (Margulis and Fester, 1991
; Herre et al., 1999; McFall-Ngai, 1999). Symbioses may be generalized, with multiple potential partners, or specialized, with a single host species and a single symbiont species. The costs and benefits of generalization and specialization have been examined for interactions between pollinators and plants (Thompson, 1994); rhizobia and legumes (Young et al., 2003); ectomycorrhizae and plants (Bruns et al., 2002); and dinoflagellates and corals (Baker, 2003; Santos et al., 2004). For many of these interactions, a high degree of host-specificity is associated with increased benefits to the host (Thompson, 1994; Bruns et al., 2002). Alternatively, many corals can host multiple types of dinoflagellates in different habitats, possibly reflecting environmental specialization by the symbionts (Rowan, 1998; Baker, 2003; Knowlton and Rohwer, 2003).
Symbiotic cyanobacteria (blue-green algae) and heterotrophic bacteria are found inside nearly all marine sponges (Wilkinson et al., 1981; Unson et al., 1994; Sarà et al., 1998; Friedrich et al., 1999). These symbionts may form a mutualism with their host sponge, especially if the symbionts provide their host with fixed carbon and/or nitrogen, while their host provides other essential nutrients and shelter (Wilkinson and Fay, 1979; Rai, 1990; Sarà et al., 1998). The biomass of photosynthetic cyanobacteria can nearly equal that of sponge cells, with up to 50% of the sponge's energy budget and 80% of the sponge's carbon budget derived from photosynthesis (Wilkinson, 1983; Cheshire et al., 1997). Many sponges gain this nutrition through the phagocytosis and digestion of their microbial symbionts (Rützler, 1988; Maldonado and Young, 1998). In addition, cyanobacterial symbionts have been implicated in the production of secondary metabolites isolated from marine sponges (Unson et al., 1994; Flowers et al., 1998; Schmidt et al., 2000). These compounds can serve a variety of ecological functions, including predator and competitor deterrence (Pawlik et al., 1995; Thacker et al., 1998; Engel and Pawlik, 2000) and resistance to malignant microbial infections (Garson, 2001; Thakur et al., 2003).
Two major groups of cyanobacterial symbionts have been reported from marine sponges, filamentous Oscillatoria spongeliae and unicellular Synechococcus spp. Oscillatoria spongeliae has been reported from three species in the family Dysideidae (Order Dictyoceratida): Lamellodysidea (formerly Dysidea) herbacea, L. chlorea, and D. granulosa (Larkum et al., 1987; Hinde et al., 1994; Thacker and Starnes, 2003). Phylogenies constructed for these three sponge species and their cyanobacterial symbionts provide strong evidence for host specificity, as each sponge species hosts a phylogenetically distinct clade of O. spongeliae (Thacker and Starnes, 2003). Synechococcus symbionts have been reported from a much wider variety of sponges, including Xestospongia muta (Petrosiidae, Haplosclerida; Gómez et al., 2002), Aplysina aerophoba (Aplysinidae, Verongida; Hentschel et al., 2002,), and Chondrilla nucula (Chondrillidae, Chondrosida; Usher et al., 2004b). Sponge-associated Synechococcus are genetically distinct from planktonic Synechococcus, but there is no evidence to suggest that these symbionts are host-specific (Usher et al., 2004a).
The impact of cyanobacterial photosynthesis on sponge metabolism can be manipulated by shading sponge-cyanobacteria associations (Sarà et al., 1998; Gómez et al., 2002). In this study, L. chlorea and X. exigua were shaded simultaneously to determine if sponges containing different cyanobacterial symbionts respond differently to reduced light availability. If photosynthetic symbionts provide a net benefit to their host sponges, shading may decrease sponge performance. If host sponges are extremely dependent on cyanobacterial photosynthesis, shading may also cause the host sponge to lose mass. Since measurements of sponge mass could potentially disturb these sponges, L. chlorea were also shaded in situ, with measurements of sponge performance based on area (percent cover). To determine whether cyanobacterial abundance changed due to shading, cyanobacterial abundance was quantified by measuring chlorophyll a concentrations in the sponges.
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MATERIALS AND METHODS |
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SYNOPSISINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Study Organisms
Lamellodysidea chlorea (Order Dicytoceratida, Family Dysideidae) and Xestospongia exigua (Order Haplosclerida, Family Petrosiidae) are common sponges in the shallow lagoons of the Republic of Palau. L. chlorea has an encrusting growth form, approximately 1 to 2 mm thick, occasionally with upright projections 2 to 4 mm wide. The surface is conulose, with conules up to 1 mm high that are distributed evenly, 1 to 3 mm apart. The skeleton of L. chlorea is a loose reticulation of spongin fibers, 25 to 80 µm in diameter, that are usually cored with sand and debris (Bergquist, 1965
); the lack of a mineral skeleton makes this sponge soft and compressible. The endosome of L. chlorea contains a large amount of filamentous cyanobacteria, Oscillatoria spongeliae (Thacker and Starnes, 2003). X. exigua has encrusting, repent, and erect growth forms, with crusts 10 to 20 mm thick, while repent and erect branches are 10 to 40 mm in diameter and can reach lengths over 30 cm, occasionally anastomosing. X. exigua possesses a mineral skeleton of siliceous spicules, whose dimensions range from 1.5 to 5.5 µm in width and 100 to 135 µm in length. These spicules are arranged in an isodictyal reticulation, with additional, ascending multispicular tracts up to 300 µm wide (Bergquist, 1965); the robust mineral skeleton of X. exigua makes this sponge quite rigid.
Identity of Xestospongia exigua symbionts
Total genomic DNA was isolated from RNAlater-preserved Xestospongia exigua using the Wizard Genomic DNA Purification Kit, following the manufacturer's protocol (Promega Corporation, Madison, WI). Cyanobacterial 16S rDNA sequences were amplified using a combination of cyanobacteria-specific and general bacterial primers as previously described (Nübel et al., 1997; Martinez-Murcia et al., 1995; Thacker and Starnes, 2003): CYA106F (5'-CGGACGGGTGAGTAACGCGTGA-3'), CYA359F (5'-GGGGAATYTTCCGCAATGGG-3'), CYA781R (5'-GACTACWGGGGTATCTAATCCCWTT-3'), and 1509R (5'-GGTTACCTTGTTACGACTT-3'). Sequences were assembled using Sequencher 4.1 (GeneCodes, Ann Arbor, MI) and aligned using the Se-Al sequence alignment program (Rambaut, University of Oxford).
Several reference sequences from GenBank were included in the alignment, including Synechococcus symbionts from the marine sponges Aplysina archeri (AF497567
[GenBank]
; Diaz, 1997), Chondrilla australiensis (AY190176
[GenBank]
, AY190177
[GenBank]
; Usher et al., 2004b), Chondrilla nucula (AY190180
[GenBank]
, AY190186
[GenBank]
; Usher et al., 2004b), and Aplysina aerophoba (AJ347056
[GenBank]
, Hentschel et al., 2002; AY190185
[GenBank]
, Usher et al., 2004a). Sequences representing planktonic Synechococcus included strains PCC 6716 (AF216942
[GenBank]
; Robertson et al., 2001), PCC 7002 (AJ000716
[GenBank]
; Nübel et al., 1997), PCC 7003 (AB015059
[GenBank]
; Honda et al., 1999), PCC 7335 (AB015062
[GenBank]
; Honda et al., 1999), PCC 7942 (AF132930
[GenBank]
; Turner et al., 1999), WH 5701 (AY172832
[GenBank]
; Fuller et al., 2003), WH 7803 (AF311291
[GenBank]
; West et al., 2001), WH 8101 (AF001480
[GenBank]
; Urbach et al., 1998), and WH 8103 (AF311293
[GenBank]
; West et al., 2001). Another member of the Chroococcales, Gloeobacter violaceus strain PCC 7421 (AP006573; Nakamura et al., 2003), was included as an outgroup. Likelihood ratio tests comparing hierarchical models of DNA substitution were evaluated by Modeltest (Posada and Crandall, 1998). A phylogenetic tree was generated in PAUP (Swofford, 1999) using the maximum likelihood distance settings calculated by Modeltest in a neighbor-joining search. Support for each node was evaluated with 500 bootstrap replicates of a neighbor-joining search.
Shading experiments
Ten individuals of each species were collected from Risong Bay and transported to the Coral Reef Research Foundation (CRRF, Koror, Palau) for initial measurements of sponge wet mass. Each individual was divided into three pieces, with one piece used for initial measurements of dry mass and chlorophyll a concentration and the remaining pieces used in the control and shaded treatments. Individuals of L. chlorea had an encrusting growth form, approximately 2 mm thick, with few upright projections; each individual was divided into roughly circular pieces approximately 8 cm in diameter. Collections of X. exigua targeted sponges with repent branches, approximately 20 mm in diameter, with each individual divided into pieces 7 to 9 cm long.
The sponges were attached to 15 cm x 15 cm rigid plastic grids (15 mm mesh; Plaskolite, Inc.) using plastic cable ties. All sponges were attached in their natural orientation, that is, the encrusting form of L. chlorea was placed on the grids with the basal side touching the grids; the repent branches of X. exigua were placed on the grids horizontally. PVC and carriage screws attached to the grids supported a 25 cm square canopy of UV and visible-light transparent Plexiglas. Shaded sponges were covered by opaque Plexiglas to reduce light availability. The grids were attached to bare substrates in Risong Bay using reef hooks and fishing line, such that the top of each canopy was fully exposed to down-welling light. Fouling organisms and sediment were removed from each replicate twice weekly. After two weeks, all replicates were collected and returned to CRRF for measurements of final sponge wet mass. Sponges were frozen and lyophilized for measurements of final sponge dry mass.
Initial dry masses were obtained by regression analyses of wet mass and dry mass samples from each of the ten source individuals. Relative changes in mass were calculated as (final-initial)/initial dry mass for each replicate. Differences in relative mass change were compared between species and shading treatments by analysis of variance (ANOVA); the data were arcsine transformed to meet the assumptions of normality (Sokal and Rohlf, 1995).
Since the abundance of cyanobacteria is directly correlated with chlorophyll a concentrations (Wilkinson, 1983; Rai, 1990), cyanobacterial abundance was estimated by measuring chlorophyll a concentrations in each specimen using a spectrophotometric technique (Parsons et al., 1984). Chlorophyll a was extracted from a weighed piece of lyophilized sponge in a 90% acetone:water mixture held overnight at 4°C. Each sample was centrifuged to remove suspended solids, after which the supernatant was transferred to a spectrophotometer cuvette, and absorbance was measured at 750, 664, 647, and 630 nm. Chlorophyll a concentrations were calculated based on equations provided by Parsons et al. (1984) and standardized to sponge dry mass. Differences in chlorophyll a concentrations due to sponge species and shading treatments were compared by ANOVA. Due to a significant interaction between species and shading treatment, post-hoc Bonferroni comparisons were used to determine whether each species showed significant variation in chlorophyll a concentration due to shading.
To control for any impacts of handling prior to the experimental manipulations, an additional set of L. chlorea was shaded in situ. For this experiment, area (measured as percent cover) was chosen as the response variable. Since the encrusting growth form of L. chlorea has a relatively uniform thickness of 2 mm, any loss or addition of mass is highly correlated with a change in the amount of area covered by the sponge. Prior to the installation of each treatment, an initial photograph of each individual was taken using a Nikonos underwater camera with a 28 mm lens and a 144 x 216 mm framer attached. A transparent or opaque Plexiglas canopy, supported by PVC and carriage screws, was placed over each individual, with ten individuals having access to light, and ten individuals shaded. These were grouped by depth and spatial location on the reef into 10 paired replicates of each treatment. After two weeks, the canopies were removed, and a final photograph was taken of each individual. To determine the final concentration of chlorophyll a, an approximately 10 square cm sample was collected from each individual.
Each photograph was digitized and then analyzed using the Image-J software package (U.S. National Institutes of Health). Non-sponge material was erased from the image, with the remaining sponge material converted to a black-and-white image. Image-J was then used to calculate the percent cover of sponge material present in the image. Relative changes in percent cover were calculated as (final – initial)/initial. Relative changes in percent cover and final chlorophyll a concentrations were compared between the two treatments using paired t-tests.
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RESULTS |
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Gene sequences (16S rDNA) of cyanobacterial symbionts amplified from X. exigua have been deposited in GenBank under accession numbers AY692243 [GenBank] to AY692245 [GenBank] . These sequences shared 99.3% identity to Synechococcus spongiarum isolated from the marine sponge Chondrilla nucula (Usher et al., 2004b
; Fig. 1). Hierarchical models of DNA substitution indicated that a general time-reversible model (Rodríguez et al., 1990) that included both the proportion of invariable sites and heterogeneous rates of substitution among variable sites best fit the data. Model parameters estimated using Modeltest (Posada and Crandall, 1998) included the substitution rate matrix (A–C = 1.06, A– G = 2.21, A–T = 1.21, C–G = 0.56, C–T = 4.64, and G–T = 1.00), the proportion of invariable sites (I = 0.56), and the gamma distribution shape parameter (G = 0.65). Bootstrap analyses strongly supported the placement of X. exigua symbionts into a monophyletic clade with other Synechococcus symbionts from marine sponges (Fig. 1). These symbionts are genetically distinct from their free-living relatives, showing 86 to 95% similarity to planktonic Synechococcus. No significant bootstrap values were found within the sponge-associated clade, providing no evidence for evolutionary specialization of Synechococcus among sponge hosts. Evidence for the evolutionary specialization of Oscillatoria spongeliae is provided by Thacker and Starnes (2003).
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While Xestospongia exigua showed very little change in dry mass in either the control or shaded treatments, Lamellodysidea chlorea lost 10.5% dry mass in the control treatment and lost 33.9% dry mass in the shaded treatment (Fig. 2). Although differences between species and treatments were statistically significant (species: F = 4.73, df = 1, P = 0.04; treatment: F = 4.37, df = 1, P = 0.04), the probability of a species x treatment interaction P = 0.09 (F = 3.10, df = 1). Initial chlorophyll a concentrations were significantly higher in L. chlorea than X. exigua (Fig. 3, F = 9.95, df = 1, P < 0.01). After two weeks of shading, final chlorophyll a concentrations showed a significant species x treatment interaction (Fig. 3; F = 6.61, df = 1, P = 0.02), indicating that the two species responded differently to the shading treatment. Post-hoc Bonferroni comparisons revealed that chlorophyll a concentrations in shaded X. exigua were lower than in controls (P = 0.03). Chlorophyll a concentrations were not significantly different between shaded and control L. chlorea (P = 0.12).
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Initial measurements of L. chlorea percent cover were not significantly different between the in situ control and shaded treatments (control: 57.2 ± 5.2%; shaded: 62.1 ± 4.3%; t = 0.79, df = 9, P = 0.45). After two weeks, control sponges increased their percent cover, while shaded sponges lost nearly half of their initial percent cover (relative change in percent cover of control sponges = 6.7 ± 5.3%; shaded sponges = –42.1 ± 11.9%; t = 4.13, df = 9, P < 0.01). Final chlorophyll a concentrations did not differ between control L. chlorea and those that were shaded (control: 684.5 ± 84.4 µg/g; shaded: 671.4 ± 77.5 µg/g; t = 0.11, df = 9, P = 0.92).
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DISCUSSION |
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Several species within the sponge family Dysideidae are known to form symbiotic associations with host-specific, filamentous cyanobacteria, Oscillatoria spongeliae (Thacker and Starnes, 2003
). Other sponges, including species of Xestospongia, Aplysina, and Chondrilla, host unicellular cyanobacterial symbionts, recently classified as Synechococcus spongiarum (Usher et al., 2004b). In this study, Xestospongia exigua was demonstrated to host S. spongiarum, and the generalist distribution of this symbiont was confirmed through a phylogenetic analysis. Field experiments with L. chlorea and X. exigua provided valuable insights on appropriate protocols for manipulating marine sponge– symbiont associations. Disturbing the extremely soft and compressible structure of L. chlorea during the initial weighing process may have led to the high mass loss observed in control sponges. The in situ shading experiment was conducted to avoid this initial disturbance, and successfully demonstrated that percent cover can be used as a measure of L. chlorea performance. X. exigua is much more robust and rigid than L. chlorea and withstood handling in the laboratory very well.
If cyanobacterial symbionts benefit their host sponges, the inhibition of cyanobacterial photosynthesis by shading is predicted to reduce this benefit, leading to decreased performance of the host sponge. For L. chlorea, shading led to a dramatic loss of sponge mass and percent cover, indicating that the Lamellodysidea–Oscillatoria symbiosis is likely a mutualistic interaction. Despite the strong impact of shading, O. spongeliae abundance did not significantly change, indicating that these symbionts may be unable to disperse from their host. However, for X. exigua, shading did not affect sponge mass; in addition, when these sponges were shaded, a loss of cyanobacterial chlorophyll a was observed. The Xestospongia–Synechococcus symbiosis may be a commensal interaction if these cyanobacteria are able to disperse from the host sponge when unfavorable environmental conditions arise. Alternatively, this symbiosis may represent a facultative mutualism, with the sponge consuming cyanobacteria that are not photosynthetically active. The fate of shaded S. spongiarum remains to be documented in future experiments. These results suggest that a higher degree of host-specificity is correlated with increased benefits to the host, an outcome that has been reported for diverse mutualisms (Thompson, 1994; Bruns et al., 2002). However, these results are based only on two sponge species; clearly, additional experiments are needed using an expanded phylogenetic and geographic sampling of species.
A potential criticism of this study is that the greater dry mass of X. exigua, due to its robust mineral skeleton, confounds comparisons with L. chlorea. Dry mass was chosen as the response variable in this experiment because there is otherwise no clear way to standardize measurements of size between these two species, since area covered by the repent branches of X. exigua is not well correlated with mass, and the volumes of the two species cannot be measured accurately prior to experimentation. Although X. exigua does contain a mineral skeleton, loss of living matter from either sponge results in a decrease in dry mass. The experiment was conducted for only two weeks because longer-term experiments resulted in the complete loss of L. chlorea. Since X. exigua contains a mineral skeleton, it may not grow as rapidly as L. chlorea; however, if sponge health declines, a loss of mass is expected. Longer-term experiments are certainly needed to address the impacts of shading on Xestospongia survival and reproduction. Gómez et al. (2002) conducted a seven-week shading experiment with X. muta, observing no change in sponge mass, but a loss of cyanobacteria from shaded sponges. These results provide additional evidence that S. spongiarum may play a commensal role in these sponges, but do not resolve the issue of low Xestospongia growth rates.
Since each partner of a symbiosis can respond to specific costs and benefits, mutualisms may represent a trade-off between conflict and cooperation (Herre et al., 1999). Local environmental conditions may mediate trade-offs between cyanobacterial symbionts and marine sponges, with environmental changes disrupting cooperation between mutualists and creating a more competitive or parasitic interaction. For example, in shaded conditions, cyanobacterial symbionts often are not found in potential sponge hosts (Rützler, 1988; Sarà et al., 1998), most likely because of the lack of available light for photosynthesis. However, as suggested earlier, it is not known whether these symbionts can disperse away from a shaded environment or whether they are more readily consumed by their hosts in shaded conditions. Rützler (1988) described cyanobacterial symbionts overgrowing their host sponges, with cyanobacteria multiplying faster than the host sponge could phagocytose or expel them. Increased water temperature and increased nutrient availability may stimulate rapid symbiont growth that cannot be controlled by the host sponge (Rützler, 1988). With a high potential for both parasitic and mutualistic interactions, sponges and their cyanobacterial symbionts may provide model systems for examining the trade-offs between the costs and benefits of symbiosis.
Dispersal ability may also play a key role in determining the extent of host specificity (Thompson, 1994). Symbionts able to disperse independently from their host may become less specialized, while symbionts that cannot disperse from their host may become more specialized. Law (1985) predicted that mutualistic endosymbionts would lack strong specificity to particular host species, as the symbionts would become so accommodating to their hosts that transfer among unrelated hosts would be favored by selection. Therefore, early in the evolution of a mutualism, endosymbionts may evolve extreme specialization, but over time, host-specificity may decrease as the endosymbiont becomes able to form associations with other hosts; however, this hypothesis relies on dispersal of symbionts among different host species (Thompson, 1994). Symbioses formed by Oscillatoria and Synechococcus may reflect these two different evolutionary stages, with Oscillatoria currently more specialized and Synechococcus more generalized. Alternatively, a lack of independent dispersal by Oscillatoria may also generate these two patterns of host specificity. To address these hypotheses, studies of the relative ages of these associations are needed. Measurements of cyanobacterial residence time (or turnover) in sponges and cyanobacterial dispersal would also enable testing of these hypotheses. In addition, it remains unclear how these symbioses can be regulated and whether this regulation has a cost for the host sponge. The extent of vertical and/or horizontal symbiont transmission also remains to be studied.
The shading experiments reported here suggest that cyanobacterial symbionts with more generalized host distributions may have less beneficial impacts on their host sponges, while more specialized host-symbiont associations are correlated with a greater benefit to the host sponge. However, this generalization may not be valid if S. spongiarum is more specialized for some sponge species. There is a clear need for broader phylogenetic analyses of the specificity of Synechococcus-sponge associations, with the use of more variable markers potentially revealing a greater degree of host specificity, as reported recently for the Symbiodinium associates of octocorals (Knowlton and Rohwer, 2003; Santos et al., 2004). Since host specificity may vary geographically and among sponge lineages, the magnitude of benefits that sponges derive from their symbionts may also vary across both geographic and evolutionary scales.
While this study considered sponge benefits at an ultimate level (measuring loss or gain of sponge mass and area), more proximate studies of these symbioses are essential to integrate sponge and symbiont physiology and to obtain better estimates of the costs and benefits to each member of these associations. Although it is known that some strains of Synechococcus can photo-acclimate to changing irradiances (Samson et al., 1994; Six et al., 2004), this phenomenon has yet to be studied in S. spongiarum, O. spongeliae, and other sponge-symbiont associations. If Synechococcus symbionts do photo-acclimate, chlorophyll a concentrations would be expected to increase in the shaded treatment (Samson et al., 1994; Six et al., 2004). Since a decrease in chlorophyll a concentrations was observed for the Xestospongia–Synechococcus association, photo-acclimation alone cannot explain these results. Chlorophyll a concentrations varied widely in the Lamellodysidea–Oscillatoria association, with no statistically significant change in the shaded treatment. Additional factors that could generate variation in chlorophyll a concentrations include interactions between cyanobacteria and other microbial symbionts, nutrient availability, and/or regulation of cyanobacterial populations by host sponges. Measurements of cyanobacterial cell numbers and photosynthetic rates would be useful to better understand the physiology of these symbionts. Although the sponges in this study contained concentrations of chlorophyll a higher than those reported by Wilkinson (1983, 1987), it is unknown whether their rates of photosynthesis compensate for sponge respiration. Measurements of photosynthesis-irradiance curves are required to compare these results to Wilkinson's (1983, 1987) observations of heterotrophic and phototrophic sponges.
As demonstrated by several other authors in this symposium, microbial symbionts of sponges are currently of great interest for their novel natural products and potential biomedical applications. These symbioses also provide model systems for exploring the costs and benefits of symbiosis and the roles of dispersal, environmental conditions, and phylogenetic history in determining the specificity of endosymbionts for their hosts. Further investigations of these symbioses will greatly enhance our understanding of the general ecological and evolutionary mechanisms that structure mutualisms and symbiotic associations.
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ACKNOWLEDGMENTS |
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Lori and Pat Colin generously shared their knowledge of marine sponges and provided field support at the Coral Reef Research Foundation. Patrick Erwin and Kevin Bevis assisted in the field and laboratory components of this project. Helpful suggestions on conducting these experiments were contributed by Valerie Paul and Mikel Becerro, while comments by Richard Helling, Frank Camacho, Alan Kohn, and two anonymous reviewers improved the manuscript. Adalbert Eledui, Kathy Chaston, and Theo Isamu are thanked for securing permits to conduct research in the Rock Islands of the Republic of Palau from the Koror State Government and the Division of Marine Resources. This material is based upon work supported by the National Science Foundation under Grant No. 0209329.
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FOOTNOTES |
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1 From the Symposium Sponges: New Views of Old Animals presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5–9 January 2004, at New Orleans, Louisiana.
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References |
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