Vol. 23: 1–13, 2014 AQUATIC BIOLOGY Published online December 2 doi: 10.3354/ab00612 Aquat Biol

OPENPEN ACCESSCCESS FEATURE ARTICLE

Trait-mediated ecosystem impacts: how morphology and size affect pumping rates of the Caribbean giant barrel sponge

Steven E. McMurray, Joseph R. Pawlik, Christopher M. Finelli*

Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, North Carolina 28403-5919, USA

ABSTRACT: Sponges are a dominant component of Caribbean coral reef suspension-feeding communi- ties. Understanding how pumping rates are affected by sponge size and morphology, as well as the en- vironment, is fundamental to understanding the ecological interactions that are mediated by sponge filtration. In a comprehensive in situ investigation of sponge pumping, the excurrent seawater velocities of 274 specimens of the largest Caribbean species, the giant barrel sponge Xestospongia muta, were measured at sites in the Bahamas and Florida Keys to investigate (1) the relationship between excurrent velocity distributions and sponge morphology, (2) the scaling relationship between pumping and sponge size, and (3) temporal variation of pumping and sensitivity to environmental changes. Excurrent velocity distributions across the osculum showed peak velocities at the center and diminishing veloci- ties near the edges of the osculum. The degree of center-weighting was explained by the distribution A diver positions an accoustic Doppler velocimeter over a of sponge biomass relative to the spongocoel. Volu- Caribbean giant barrel sponge Xestospongia muta to mea - metric pumping rates scaled isometrically with sponge sure the velocity of seawater pumped by the sponge. −1 −1 size and averaged 0.06 ± 0.04 l s l sponge tissue, Photo: Steven McMurray but were reduced for extremely large sponges. Pumping activity was relatively constant over short temporal scales, but varied over longer scales; how- ever, variations in pumping rates, in cluding periods INTRODUCTION of cessation, were asynchronous across the pop - ulation and uncorrelated with changes in environ- Benthic suspension feeders are important compo- mental conditions. We estimate that populations of nents of marine ecosystems (Gili & Coma 1998). X. muta in the Florida Keys and Bahamas process a They efficiently process large volumes of water and volume of water equivalent to a layer 1.7 to 12.9 m thick each day and overturn the water column every thereby play important roles in benthic−pelagic cou- 2.3 to 18.0 d. pling (Pile et al. 1997, Bak et al. 1998), organic matter cycling (Reiswig 1974, Yahel et al. 2003) and nutrient KEY WORDS: Volume flow · Porifera · Scaling · element cycling (Southwell et al. 2008, Fiore et al. Water column turnover · Water velocity 2013). By modifying the biotic and abiotic properties

© The authors 2014. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 2 Aquat Biol 23: 1–13, 2014

of seawater, benthic suspension feeders mediate a found to remove 1870 mg C d−1 m−2 of prokaryotic number of direct and indirect ecological interactions. picoplankton, resulting in a picoplankton-depleted In shallow-water systems, and where they occur in layer of water within 1 m of the benthos, but were a dense assemblages, benthic suspension feeders may source of 750 mg C d−1 m−2 of eukaryotic picoplank- control phytoplankton biomass, thereby clarifying ton (Pile et al. 1997). Sponges are also important in the water and increasing light availability to eco - nitrogen cycling and release large amounts of dis- logically important benthic autotrophs (Cloern 1982, solved inorganic nitrogen that may influence levels Officer et al. 1982). On coral reefs, benthic suspen- of primary production on coral reefs (Southwell et al. sion feeders can deplete phytoplankton concentra- 2008, Fiore et al. 2013). Mass mortality of the Florida tions in overlying waters and represent an important Bay sponge community resulted in an increase in the pathway for the retention of allochthonous carbon average water column turnover rate by as much as and nutrients in coral reef ecosystems (Yahel et al. 12 d for some regions of the Bay and could account 1998, Monismith et al. 2010). for the increased algal blooms reported there (Peter- Sponges are benthic suspension feeders with a son et al. 2006). More recently, sponges have been body plan that is specialized to actively pump large described as essential to the cycling of carbon on volumes of seawater (Larsen & Riisgård 1994). Water coral reefs via the ‘sponge loop’, whereby sponges enters the sponge through numerous incurrent pores, consume dissolved organic matter and make carbon or ostia, which line the sponge surface, and then available to other reef fauna in the form of detritus flows through a series of branching and successively (de Goeij et al. 2013). narrowing incurrent canals to the water-pumping Sponges are found across a diversity of marine units, the choanocyte chambers. From here, water habitats, but are particularly dominant benthic sus- subsequently flows through a series of excurrent pension feeders on Caribbean coral reefs, where their canals that merge and empty into the atrial cavity, biomass surpasses that of any other benthic group the spongocoel, then to an excurrent osculum or os - (Díaz & Rützler 2001). Further, there is mounting evi- cula (Larsen & Riisgård 1994). Volume flow through dence that sponges may be increasing in abundance sponges has been estimated to range from 0.005 to on coral reefs (Colvard & Edmunds 2011, Ruzicka et 0.034 l s−1 l−1 sponge tissue for Aplysina lacunosa to al. 2013). For example, populations of the giant barrel 0.578 l s−1 l−1 sponge tissue for Callyspongia vaginalis sponge Xestospongia muta in the Florida Keys in - (Weisz et al. 2008), and water column turnover esti- creased by 46% between 2000 and 2006, and models mates can range from <1 to 56 d for sponge assem- indicate that populations will continue to increase blages at naturally occurring densities (Reiswig 1974, (McMurray et al. 2010). Given forecasts of the nega- Pile et al. 1996, Savarese et al. 1997). tive effects of global warming and ocean acidification Pumping activity is required for sponges to feed on reef-building corals, sponges may become increas- and respire and is therefore strongly connected to ingly more dominant on Caribbean coral reefs, and sponge physiology and ecology. High excurrent sea - their roles in mediating water column processes may water velocities that ensure the separation of incur- become even more substantial (González-Rivero et rent and filtered seawater may be necessary for al. 2011, Bell et al. 2013). sponges to occupy low-flow habitats (Bidder 1923, To address needs for the implementation of Reiswig 1971, Riisgård et al. 1993). Sponges working ecosystem-based approaches to coral reef manage- at high internal pressures may be more susceptible to ment (NOAA 2007), a greater understanding of the occlusion of the aquiferous system by sediment in eco logical processes mediated by sponges through low-energy habitats (Reiswig 1971). Pumping rates their interactions with the water column is required. are also indicative of sponge life-history strategies De tailed quantitative measurements of sponge and phenotype: sponge species with high microbial pumping are necessary to scale material (e.g. carbon, abundances (HMA) typically have a denser mesohyl, nu trients) flux estimates from individuals to pop - more complex aquiferous systems, lower densities of ulations and to estimate the magnitude of sponge- choanocyte chambers, possibly different feeding stra- mediated material fluxes. In this study, we investi- tegies, and lower pumping rates relative to low micro- gated the pumping rates of the giant barrel sponge bial abundance (LMA) species (Weisz et al. 2008). X. muta, a particularly dominant Caribbean coral The pumping activities of sponges also mediate reef sponge. X. muta is a large and long-lived species numerous water column processes (Maldonado et that can comprise up to 65% of the total sponge bio- al. 2012). For example, Baikalospongia bacillifera mass on some reefs (McMurray et al. 2008, Southwell and B. intermedia from Lake Baikal, Russia, were et al. 2008) and is the second most common sponge McMurray et al.: Pumping rates of Xestospongia muta 3

across the Caribbean on the basis of percentage cover (Loh & Pawlik 2014). Our objectives were to determine how sponge size and morphology influ- ence sponge pumping rates, and to determine how pumping may vary over time and with environmental changes. Results of this study are important in pro- viding a foundation for subsequent quantitative work on the material fluxes mediated by sponges and will enable managers to better understand and predict the ecological consequences of those fluxes.

MATERIALS AND METHODS

Study sites

Pumping rates of Xestospongia muta were studied at sites in the Florida Keys (Conch Reef, 24° 56.9’ N, 80° 27.2’ W and Pickles Reef, 24° 59.2’ N, 80° 24.6’ W) and the Bahamas (Great Stirrup Cay, 25° 49.6’ N, 77° 53.9’ W; Little San Salvador, 24° 34.7’ N, 75° 57.6’ W; Fig. 1. The giant barrel sponge Xestospongia muta with an Plana Cays, 22° 36.4’ N, 73° 37.5’ W; San Salvador, acoustic Doppler velocimeter (ADV) probe positioned over 24° 3.3’ N, 74° 32.5’ W; and Sweetings Cay, 26° 34.1’ N, the sponge osculum to measure the velocity of excurrent 77° 53.4’ W). Water depths ranged from 15 to 30 m. seawater. Photograph: S. E. McMurray Aquarius Reef Base and the R/V ‘Walton Smith’, and the R/V ‘Seward Johnson’ were used as platforms (ADV) mounted on a tripod. The ADV probe was for SCUBA diving at sites in the Florida Keys and positioned vertically over each sponge (Fig. 1) so that Bahamas, respectively, over the course of 4 expedi- the sample volume was located on the plane of the tions from 2007 to 2010. At each site, sponges repre- sponge osculum (Finelli et al. 1999a). For each senting a broad range of sizes (17.8 to 451 649 cm3) sponge, ex current velocity was measured at the were selected for study; however, only individuals osculum centerline (wcenter) and at points (4 to 11, with a single osculum and with no obvious signs of depending on the size of each sponge osculum) disease or tissue damage were included. Addition- approximately every 3 cm across the osculum for ally, individuals fouled with algae or colonized by 3 min at 5 Hz. Following excurrent velocity measure- zoanthids were excluded, as epibionts have been ments, sponge height, base circumference, osculum shown to reduce sponge pumping rates (Lewis & diameter, spongocoel depth and spongocoel base Finelli 2014). The proportion of sponges excluded diameter were measured with a flexible plastic from our study due to disease or fouling was <2% at measuring tape and calipers. For size and morphol- all sites; the proportions of multi-oscula sponges at ogy estimates, sponge and spongo coel volumes were our study sites ranged from <1 to 11%. Before and approximated as a frustum of a cone, and areas of during all pumping measurements, no physical con- oscula and spongocoel bases were approximated as tact was made with sponges. circles (McMurray et al. 2008). Theory holds that 2 distinct velocity distributions, plug and parabolic, form the endpoints of a contin- Distribution of velocities across the osculum uum exhibited as fluid flows through a pipe (Vogel 1994). For plug flow, velocities are equal across the – In order to obtain precise estimates of sponge osculum plane and w is equal to wcenter. As fluid con- pumping rates, the mean excurrent velocity of flow tinues to flow in a rigid pipe, the effects of viscosity from a sponge (w–, cm s–1) must be determined, which and friction ultimately produce flow for which the can be estimated from the distribution of velocities distribution of velocities is parabolic where w– is equal across the osculum plane. Profiles of excurrent veloc- to one-half of wcenter. Notably, while water exiting the ities across the oscula of 10 sponges were measured sponge osculum is not strictly analogous to flow using a Sontek Micro acoustic Doppler velocimeter through a rigid pipe, initial measurements suggested 4 Aquat Biol 23: 1–13, 2014

that the cross-osculum distributions of velocity were Unlike some sponge species that may contract – center-weighted such that w was a fraction of wcenter. (Reiswig 1971), the osculum of X. muta is rigid and Therefore, profiles of excurrent velocities across the invariant; therefore, volume flow (i.e. pumping rate) osculum were integrated gravimetrically to deter- through each sponge was calculated as: mine w– by weighing velocity by the percent of the Q = w– × A (1) total osculum area between successive measurement osc points (Reiswig 1974). Because the morphology of the where Q is volume flow (ml s−1). The relationship spongocoel has been shown to influence velocity between Q and Vsponge was described by the allo - profiles (Reiswig 1974), linear regression was used to metric equation: determine the relationship between osculum dia- α β – Q = Vsponge (2) meter and the ratio of w to wcenter as well as the rela- 2 tionship between the ratio of osculum area (Aosc, cm ) Data were log10 transformed and RMA regression 2 – to spongocoel base area (Asb, cm ) and the ratio of w was performed to determine the scaling coefficient, to wcenter. For both regressions, variables were natu- α, and the scaling exponent, β of Eq. (2) (Warton et al. ral log transformed and ordinary least squares 2006). The T statistic was used to test the actual slope regression was used because a predictive relation- against an isometric slope of β = 1 (McArdle 1988). ship was sought (Warton et al. 2006). ANCOVA was used to test for differences in Q be -

tween sites with Vsponge as the covariate and site as a fixed factor. Scaling of pumping rates with sponge tissue volume The cycle time (sensu Reiswig 1974), or time re - quired for a sponge to pump a volume of water The excurrent velocities and physical dimensions of equivalent to its volume, for each sponge was calcu- a total of 235 sponges were measured to examine how lated by dividing Vsponge by Q. Water-column trans- pumping rates of X. muta scaled with sponge size. Ex- port rates for populations of X. muta were calculated current seawater velocities were measured using as the product of the mean biomass of X. muta per either a Sontek MicroADV or Nortek ADV mounted unit area and the mean rate of volume flow found on tripods with the ADV probe centered over the here (0.06 l s−1 l−1). The biomass of X. muta at Sweet- sponge and oriented such that wcenter was measured. ings Cay (n = 5) and San Salvador (n = 4), Bahamas, Excurrent velocities of each sponge were measured was estimated by measuring the size of all single- over a 2 to 3 min sampling period at 4 or 5 Hz. Follow- osculum individuals within haphazardly placed repli- ing velocity measurements, the dimensions of each cate 10 m diameter circular transects. For sites in the sponge were measured as described above. Florida Keys, biomass estimates were obtained from In addition to examining how excurrent velocity the literature: 1488 cm3 m−2 for the population on was distributed across the osculum, we explored how Conch Reef in 2006 over 15, 20, and 30 m depths excurrent velocity and volumetric pumping scaled (McMurray et al. 2010), and 1609, 2100, and 960 cm3 with sponge morphology. For example, if the number m−2 for populations on offshore reefs in the Upper, of choanocyte chambers increases proportionally with Middle, and Lower Florida Keys, respectively, in 3 sponge volume (Vsponge, cm ) and all are active at the 2007 (Bertin & Callahan 2008). The estimated time same time under the same pressures, w– is expected to for these populations to overturn a water column scale linearly with sponge size. Similarly, for a given 30 m deep was calculated as the ratio of the water – excurrent volume flow, w should increase as Aosc de- column depth (i.e. 30 m) and the estimated water creases. Additionally, results from velocity profiles in- column transport rates. We note that the biomass dicated that w– is affected by spongocoel morphology estimates reported here for sites in the Bahamas and such that, for a given sponge size, w– increases as the those reported for Conch Reef, Florida (McMurray et ratio of Asb to Aosc increases (i.e. the spongocoel be- al. 2010) do not include the biomass of multi-oscula comes more cylindrical rather than conical). To test individuals (<11% of the population); thus, water these hypotheses, w– was first plotted against the ratio column transport and turnover rates for these sites of Vsponge to Aosc and reduced-major-axis (RMA) regres- are conservative estimates. sion was used to describe the relationship. The fit of X. muta harbors cyanobacterial symbionts in peri- this regression was then compared with the RMA re- ph eral tissues that impart a reddish-brown coloration – gression ofw versus the ratio of (Vsponge/Aosc)/(Aosc/Asb) to individuals; however, individuals may lose sym- to examine the change in the variation of w– explained bionts and appear bleached (McMurray et al. 2011). by considering sponge morphology. Although available evidence suggests that this type McMurray et al.: Pumping rates of Xestospongia muta 5

of bleaching is not a stressful condition, the pigmen- RESULTS tation of a subset of sponges studied was scored as either normal or bleached to investigate the relation- Profiles of excurrent seawater velocities across ship between pumping rates and sponge bleaching the osculum plane of Xestospongia muta were non- – (McMurray et al. 2011). A 1-way ANCOVA with uniform, with ratios ofw to wcenter ranging from 0.16 to Vsponge as the covariate and bleaching as a fixed 0.92 (mean ± SD = 0.46 ± 0.29, n = 10). Those profiles – factor was conducted to test for differences in Q with w to wcenter ratios ~1 were plug-like, those with between bleached and unbleached sponges. ratios ~0.5 were parabolic, and those with ratios <0.5 were strongly center-weighted with diminished flows near the osculum edges. There was no relationship Temporal variation in pumping and environmental between profile velocity distributions and sponge oscu- variables lum diameter (p = 0.49); however, the ratio of w– to

wcenter was found to allometrically decrease as Aosc 2 Long-term measurements of sponge pumping were increased relative to Asb (r = 0.60, p = 0.008, n = 10) conducted to examine temporal variation in pumping (Fig. 2). The allometric equation relating the ratio of w– rates and the sensitivity of pumping to environmental to wcenter to the ratio of Aosc to Asb was determined to be: changes. ADVs were positioned over sponges as de - −052. w ⎛ Aosc ⎞ scribed above to measure wcenter for 2 to 4 min inter- = 173. (3) w ⎜ A ⎟ vals every 3 to 10 min at 4 to 5 Hz. Measurement center ⎝ sb ⎠ periods ranged from 15 to 60 h; of the 29 sponges and this relationship was subsequently used to cor- measured, 26 were measured for >22 h, 11 were rect all excurrent velocities for the non-uniform dis- measured for >30 h, and 4 sponges were measured tribution across the osculum of each sponge. Eq. (3) for >46 h. During each deployment, excurrent ve- indicates that the distribution of velocities across the locities of 2 to 4 sponges were measured simultane- osculum become more uniform as the spongocoel ously with multiple ADVs. Following excurrent velo - becomes more cylindrical, rather than conical. Plug – city mea surements, the physical dimensions of each flow (i.e. w = wcenter) results when Aosc is approxi- – sponge were measured as described above. mately 2.87 times Asb, near-parabolic (i.e. w = 0.5 × Seawater temperature was measured by each ADV wcenter) flow occurs at Aosc to Asb ratios ~10, and – within 1 m of each observed sponge. Additional strongly center-weighted flow (i.e. w < 0.5 × wcenter) concurrent measurements of turbidity, dissolved oxy- occurs at Aosc to Asb ratios >10. The relationship be - gen, conductivity, pH, and pressure were made using tween spongocoel morphology and excurrent flow a Eureka Environmental Engineering Manta Multi- (Eq. 3) was found to be explained by the partitioning probe mounted on a tripod and placed within 10 m of measured sponges. Measurements of ambient cur- 1.0 rents were made using a Nortek Aquadopp acoustic Doppler profiler deployed on the seafloor adjacent to the area where sponge pumping was measured. 0.8 Times of sunrise and moonrise, as well as sunset and moonset during measurement intervals for each site 0.6 were obtained from the Astronomical Applications Department of the United States Naval Observatory. Time series analysis was applied to pumping and 0.4 environmental data to determine any periodicities over time (Box et al. 1994). Analysis of the cross- 0.2 spectral densities was used to investigate the relation- velocity centerline osculum ship between pumping and environmental variables Ratio of mean excurrent velocity to velocity of mean excurrent Ratio 0.0 (Finelli et al. 1999b). Differences in the standard 0102030405060 deviation of excurrent velocity at night versus day Ratio of sponge osculum area to spongocoel base area were tested with a 2-way mixed model ANOVA with sponge as a random factor and daylight as a fixed Fig. 2. Relationship between excurrent velocity distributions and spongocoel morphology, showing the ratio of mean factor. Analyses were conducted with SAS (version excurrent velocity (w– ) to velocity at the osculum centerline 9.1.3 for Windows; SAS Institute) and SPSS (version (wcenter) vs. the ratio of sponge osculum area (Aosc) to spongo- 14.0.0 for Windows; SPSS) statistical software. coel base area (Asb). Fitted line is Eq. (3) 6 Aquat Biol 23: 1–13, 2014

of sponge biomass relative to the spongocoel (see the 20 )

Supplement at www.int-res.com/articles/ suppl/b023 –1 p001_supp.pdf). Mean excurrent velocities ranged from 0.03 to 15 13.66 cm s−1 and increased linearly as a function of the ratio of V to A (r2 = 0.27, p < 0.001, n = 235). sponge osc 10 Much more of the variation in w– was explained when spongo coel morphology was additionally considered by standardizing the ratio of Vsponge to Aosc by the ratio – 5 of Aosc to Asb (w = 0.22 [Vsponge/Aosc]/[Aosc /Asb] + 1.46) 2 (r = 0.5, p < 0.001, n = 235) (Fig. 3). While pumping Mean excurrent velocity (cm s activity was relatively constant during the 3 min inter- 0 vals over which measurements were made, excurrent 020406080 Ratio of sponge volume per osculum area to velocities were found to vary over longer temporal osculum area per spongocoel base area scales (see below). To examine how this variation af- – – Fig. 3. Scaling relationship between excurrent velocity and fected estimates of w, we re gressed w computed for sponge size and morphology: mean excurrent velocity (w– ) all long-term ADV deployments (15 to 60 h) against vs. the ratio of sponge volume (Vsponge) to osculum area (Aosc) the ratio of (Vsponge /Aosc)/(Aosc /Asb). Consideration of standardized to the ratio of Aosc to spongocoel base area (Asb) the long-term temporal variation of pumping activity by sponges further increased the amount of variation inw– explained by sponge and spongocoel morphology 20000 (r2 = 0.65, p < 0.001, n = 29). )

Tissue volumes of measured sponges ranged from –1 s 17.8 to 451 649 cm3. Volume flow increased isometri- 3 15000 cally with increasing sponge volume and is reliably predicted from sponge volume (T = 1.33, df = 170, 10000 r2 = 0.78, p < 0.001) (Fig. 4). The equation relating Q to Vsponge was determined to be: 5000 Volume flow (cm 1.1 Q = 0.02V sponge (4) 0 The mean (±SD) volume flow, standardized to sponge 0 100000 200000 300000 400000 500000 −1 −1 tissue volume, was 0.06 ± 0.04 l s l . RMA regres- Sponge volume (cm3) sion of Q computed for all long-term pumping meas- Fig. 4. Volume flow (Q) vs. sponge volume (Vsponge); solid fit- urements against Vsponge was found to increase the ted line is the allometric equation (Eq. 4), dashed fitted line 2 amount of variation in Q explained by Vsponge (r = is a 4-parameter Weibull curve. Triangles indicate the 3 0.82, p < 0.001, n = 29). There was no significant dif- largest individuals that had reduced pumping rates relative to all other individuals ference in volume flow between sites (F6,227 = 1.36, p = 0.23) or between bleached and unbleached sponges (F1,163 = 0.07, p = 0.80). The mean (±SD) cycle time for X. muta was deter- While an isometric relationship was found between mined to be 30 ± 33 s. The biomass of X. muta was 3 −2 Q and Vsponge, further inspection of the data revealed determined to be 321 ± 293 cm m off Sweetings that Q was reduced for 3 to 5 of the largest individu- Cay and 2480 ± 1612 cm3 m−2 off San Salvador; water als measured (Fig. 4). The removal of the 3 largest transport rates at these sites were 1.7 and 12.9 m d−1, individuals from the dataset did not significantly respectively. Populations of X. muta on Conch Reef change the results of the regression of Q versus and on reefs in the Upper, Middle, and Lower Florida 2 Vsponge (T = 1.47, df = 168, r = 0.77, p < 0.001). Addi- Keys were found to transport water at rates of 7.7, tionally, 4-parameter log-normal and Weibull curves 8.3, 10.9, and 5.0 m d−1, respectively. Given these were fit to the data using non-linear regression. Only rates, populations of X. muta were estimated to over- the fit of the Weibull curve (r2 = 0.78, p < 0.001) was turn a water column 30 m deep every 3.9, 3.6, 2.8, comparable to that found for Eq. (4) (Fig. 4); however, and 6.0 d on Conch Reef and the Upper, Middle, and given the complexity of the Weibull function, Eq. (4) Lower Florida Keys, respectively. Water column turn- was chosen as the most parsimonious model to over estimates were 18.0 d for X. muta off Sweetings describe sponge pumping. Cay and 2.3 d for X. muta off San Salvador. McMurray et al.: Pumping rates of Xestospongia muta 7

Spectral analysis of long-term excurrent velocity The ranges of environmental variables measured measurements indicated pumping was relatively con- over long-term sponge pumping measurements were stant over time for the majority of sponges measured temperature (24.8 to 29.7°C), pH (8.0 to 8.9), conduc- (Fig. 5), but there were exceptions to this generality. tivity (54.7 to 55.6 mS cm−1), turbidity (−0.9 to 5 NTU), The largest variation in pumping occurred for 3 and dissolved oxygen (4.7 to 7.7 ppm). Excurrent sponges that demonstrated a nearly simultaneous de - velocities and environmental variables were found to −1 crease in wcenter by 12 to 16 cm s over a 32 h meas- vary over periods corresponding to the tides (Fig. 8); urement interval (Figs. 5 & 6A). The decrease in however, cross-spectral analysis of long-term excur- pumping activity started at approximately sunset, rent velocity and environmental data indicated that continued through sunrise, and corresponded with a no one parameter could explain pumping variation decrease in dissolved oxygen and pH (Fig. 6). Near by sponges. Both positive and negative correlations the end of this interval, complete cessation of pump- were found between excurrent velocities and envi- ing occurred for 1 sponge (sponge ID 2) for 10 min ronmental variables, but these correlations were not and another sponge (sponge ID 1) had significantly consistent between sponges or over similar ranges reduced or no pumping for nearly 3 h before pump- of environmental variables. In addition, simultaneous ing resumed (Fig. 6A). Pumping cessation for sponge measurements on multiple sponges, within close prox - ID 1 was associated with an increase in temperature, imity to each other and under similar environmental dissolved oxygen, and pH (Fig. 6). conditions, often revealed asynchronous temporal Rapid decreases in pumping and near or total ces- pumping patterns between adjacent sponges (Fig. 7). sation of activity was observed for 6 sponges. Pump- There was no relationship between excurrent veloci- ing cessation typically occurred at night, with pump- ties and ambient currents, lunar cycles, or daylight. ing activity resuming just before sunrise (e.g. sponge ID 5, Fig. 7). For 3 of these sponges, decreases were brief, lasting approximately 10 min, and pumping DISCUSSION was observed to recover to prior levels thereafter. For the remaining 3 sponges, pumping cessation lasted Pumping rates and sponge size between 100 and 230 min before recovery. With the exception of the sponges measured in Fig. 6A, pump- The active pumping of water is central to sponge ing cessation was not synchronous between neigh- biology and has important implications on all levels of boring sponges (Fig. 7). ecological organization ranging from that of the indi- vidual (e.g. physiology) to entire ecosystems (e.g. carbon cycling). Moreover, given current 104

and projected future states of coral reef eco-

*

* * systems (Hoegh-Guldberg et al. 2007), there 103 is a particular need to understand the magni- tude of interactions mediated by sponges through the water column. Despite this and 102 the development of advanced instrumenta- tion to measure water velocity (e.g. ADVs), 101 there have been surprisingly few compre- hensive in situ studies of sponge pumping rates since the pioneering work of Reiswig 100 (1971, 1974). Although, on an individual

Power spectral density Power spectral level, the excurrent velocities of Xestospongia 10–1 muta were found to be influenced by sponge size and morphology, our measurements on 274 sponges at sites in the Florida Keys 10–2 0102030405060and Bahamas indicate that the volume of Period (h) seawater (i.e. pumping rates) processed by sponges is largely explained and can be pre- Fig. 5. Power spectral density (log-scale) vs. period for all long-term mean excurrent velocity measurements (n = 29). Asterisks denote the 3 dicted from simple measurements of sponge sponges with the greatest variation in pumping; excurrent velocities size. The relationship between pumping rates of these sponges are plotted over time in Fig. 6A and sponge size reported here can be applied 8 Aquat Biol 23: 1–13, 2014

18 by current and future coral reef monitoring efforts A 16 (e.g. Ruzicka et al. 2013) to obtain a better un - )

–1 derstanding of the magnitude of the influence of 14 sponge populations on ecological processes mediated through the water column. 12 Given the mean rate of volume flow reported here 10 and biomass estimates from McMurray et al. (2010), we estimate that the population of X. muta on Conch 8 Reef, Key Largo, Florida processes a volume of water 6 equivalent to a water layer 7.7 m thick every day sp 1 (i.e. 7700 l m−2 d−1). Water transport rates ranged 4 sp 2 from 1700 l m−2 d−1 for X. muta off Sweetings Cay Excurrent velocity (cm s −2 −1 2 sp 3 to 12 900 l m d for X. muta off San Salvador, Bahamas. Using biomass estimates from a 0 long-term coral reef monitoring program 16.0 10 (Bertin & Callahan 2008), populations in the Temp B Florida Keys are estimated to overturn a 29.4 Press 15.8 8 water column 30 m deep every 2.8 to 6.0 d. Turb Estimates of water column turnover for popu- 29.3 lations of X. muta in the Bahamas ranged 15.6 6 from every 2.3 to 18 d. We do note that, 29.2 although sponge size is a significant predic- 15.4 4 tor of pumping rates, these estimates do not 29.1 account for temporal variations in pumping Depth (m) 15.2 2 activity. Nonetheless, these rates for a single 29.0 Turbidity (NTU) sponge species are significant when com- Temperature (°C) pared to estimates of water transport for the 15.0 0 28.9 entire sponge community on the reefs of Dis- covery Bay, Jamaica, which range between 28.8 14.8 –2 16.5 and 40 m d−1 (Reiswig 1974). If recent demographic trends of X. muta continue C 6.4 55.4 (McMurray et al. 2010), we predict that pop-

8.88 ) ulations of X. muta will exert an even greater 6.2 55.2 –1 influence over water column processes on coral reefs of the future. 8.84 6.0 55.0 Volume flow was found to scale isometri- cally with sponge biomass, indicating that 8.80 5.8 54.8 numbers of choanocyte chambers are pro-

pH portional to tissue volume. This supports 5.6 54.6 8.76 experimental work that demonstrated a cor- 5.4 54.4 relation between pumping rates and choano - Conductivity (mS cm

pH Dissolved oxygen (ppm) cyte chamber density (Massaro et al. 2012) 8.72 DO 5.2 54.2 and is consistent with the view of sponges as Cond functionally clonal organisms (Vermeij 1993). 8.68 5.0 54.0 Interestingly, however, 3 to 5 extremely large 0 240 480 720 960 1200 1440 1680 1920 individuals, uncommon on most coral reefs, Time (min) had pumping rates that were proportionally Fig. 6. Long-term 10 min means of (A) excurrent velocity at the oscu- less than smaller sponges. Sampling was lum centerline (wcenter) for the 3 sponges (sp 1, 2, and 3) with the great- limited by the availability of massive indi - est temporal variation in pumping, and simultaneous measurements of viduals, so the generality of this pattern (B) temperature (Temp), pressure (Press), and turbidity (Turb), and (C) is unclear. Nonetheless, the decrease in pH, dissolved oxygen (DO), and conductivity (Cond) plotted over time. Solid vertical line indicates time of sunset; dashed vertical line pumping observed for these individuals may indicates time of sunrise reflect a physiological size limit (Reiswig McMurray et al.: Pumping rates of Xestospongia muta 9

600 A 8 500 ) –1 6 400

300 4

200

2 sp 4 100

Excurrent velocity (cm s velocity Excurrent sp 5 sp 6 sp 7 0 0 360 720 1080 1440 1800 2160 2520 2880 4.0 Time (min) B Fig. 7. Long-term 10 min means of excurrent velocity at the 3.5 osculum centerline (wcenter) over time for 4 sponges (sp 4, 5, 6, and 7). Velocity measurements for sponges 6 and 7 do not 3.0 span the entire time interval. Solid vertical lines indicate time of sunset; dashed vertical lines indicate time of sunrise 2.5

2.0

1974, Riisgård et al. 1993) or other factors associated Temp 1.5 with the greater age of these individuals (McMurray DO et al. 2008). Additionally, sponge volume estimates Power spectral Powerdensity spectral 1.0 Press de rived here for the largest individuals may overesti- mate the volume of live tissue if the biomass of these 0.5 individuals is disproportionally occupied by sand, symbionts (e.g. polychaetes), or other non-living com- 0.0 ponents. Within 4 species investigated by Reiswig 0.12 (1974, 1981), pumping rates were nearly constant C across a range of body sizes for 3 species, although the largest specimens of Verongia reiswigi (V. gigan- 0.10 tea in Reiswig 1974) had lower tissue-specific pump- ing rates, while pumping rates generally decreased 0.08 with sponge size for Aplysina fistularis (V. fistularis in Reiswig 1981). pH 0.06 The mean specific volume flow of 0.06 ± 0.04 l s−1 Turb l−1 reported in this study is similar to the mean of Cond 0.078 l s−1 l−1 found for 5 individuals of X. muta in the 0.04 Florida Keys (Weisz et al. 2008) and 0.044 ± 0.007 l s−1 −1 l found for 22 individuals at sites in the Florida Keys 0.02 and Bahamas (Lewis & Finelli 2014). Pumping rates for X. muta are generally similar to those reported for other HMA sponges, which are consistently lower 0.00 –5.0 –4.5 –4.0 –3.5 –3.0 than those for LMA sponges (Weisz et al. 2008). The Log frequency (Hz) mean (±SD) cycle time, or time required for a sponge to pump a volume of water equivalent to its volume, Fig. 8. Mean (±SD) power spectral density estimates vs. log frequency for long-term records of (A) excurrent velocities was determined to be 30 ± 33 s for X. muta. The cycle at the osculum centerline (wcenter), (B) temperature (Temp), times for the HMA species V. reiswigi and Tecti- dissolved oxygen (DO), and pressure (Press), and (C) pH, tethya crypta (Tethya crypta in Reiswig 1974) were turbidity (Turb), and conductivity (Cond) 10 Aquat Biol 23: 1–13, 2014

approximately 19 and 22 s, respectively (Reiswig larger ranges of sizes and morphologies of X. muta 1974). Despite having relatively lower pumping rates compared to other species considered. per unit tissue volume than many LMA species, the Despite early recognition that excurrent velocity biomass of X. muta exceeds that of all other species distributions are affected by the morphology of the (Southwell et al. 2008); thus, this one dominant spe- spongocoel (Reiswig 1974), an explanation of this cies may have a disproportionate effect on water relationship has been lacking. Our model of sponge column processing. morphology and flow (see the Supplement at www.int-res.com/ articles/ suppl/b023 p001_ supp.pdf ) closely approximated the relationship observed be - Excurrent seawater velocities and sponge tween spongocoel morphology and velocity distribu- morphology tions, and suggests that the partitioning of sponge biomass relative to the spongocoel influences excur- Our measurements of pumping by X. muta re- rent water flow. According to the model of sponge vealed a close association between sponge form morphology and flow, changes in the morphology of (i.e. size and morphology) and function. Results indi- the spongocoel are concomitant with changes in the cate that distributions of velocities across the sponge distribution of sponge biomass between wall and osculum are more typically non-uniform (near- base regions of the sponge that drain excurrent flow parabolic) but velocity profiles spanned the spectrum through the peripheral and central regions of the from near-plug flow to strongly center-weighted. osculum, respectively. Sponges with larger osculum Velocity profiles were not correlated with the dia - area to spongocoel base area ratios (i.e. v-shaped meter of the osculum, suggesting that the effects of spongocoels) tend to have more biomass partitioned viscosity and wall friction are negligible. Rather, the in walls relative to the base region. However, be - morphology of the spongocoel, specifically the ratio cause the osculum is much wider for v-shaped of the areas of the osculum and spongocoel base (i.e. spongo coels relative to cylindrical spongocoels, the degree to which the spongocoel was cylindrical excurrent seawater from sponge walls exits a much rather than conical), largely determines velocity larger area of the osculum and velocity is reduced distributions. The large range of excurrent profiles relative to that at the centerline, resulting in para- reported here emphasizes the need for such meas- bolic-like flow. The implication of this relationship urements to accurately estimate sponge pumping is that sponges with v-shaped spongocoels have re- rates. For example, the mean pumping rate for 12 duced w– relative to sponges of similar biomass with specimens of X. muta on Conch Reef, Florida, and cylindrical spongocoels. Lee Stocking Island, Bahamas, estimated by Fiore et It is unclear why such large variation in spongocoel al. (2013) by measuring the speed of dye fronts at the morphologies occurs, independent of sponge size, osculum centerline and assuming plug flow (0.12 ± given the effects of morphology on excurrent sea - 0.13 l s−1 l−1; calculated from data in Fiore et al. 2013, water velocities. The speed at which water is ejected their Table 1) is double the mean pumping rate found from the osculum has been hypothesized to be impor- in the present study. tant in the separation of incurrent and filtered water This is the first study since the work of Reiswig (Bidder 1923, Riisgård et al. 1993). It is likely that (1974) to directly investigate the relationship be - ambient currents of habitats where X. muta typically tween spongocoel morphology and excurrent flow. occur are of sufficient strength to provide individuals Profile correction factors for Mycale laxissima (Mycale a continuous supply of unfiltered seawater (e.g. Moni- sp. in Reiswig 1974) ranged between 0.88 and 0.98 smith et al. 2010). However, it remains to be seen if and were found to become more parabolic as the morphological differences reflect spatial variability ratio of osculum diameter to spongocoel diameter of the flow regime across coral reefs. Morphological increased and approached 1 (Reiswig 1974). Profiles variation in X. muta may also indicate adaptation to a of V. reiswigi and Haliclona permollis were also cen- number of other environmental factors (Meroz-Fine ter-weighted, with correction factors of 0.86 and 0.58, et al. 2005). Individuals of X. muta with divergent respectively, but a relation with spongocoel morpho- external morphologies have been shown to have logy was not reported (Reiswig 1974, 1975). There is different haplotypes; therefore, it may be that mor- a paucity of available comparative data, however, the pho logy is largely genetically determined (López- range of velocity distributions for X. muta w– = 0.16 Legentil & Pawlik 2009). Similarly, differences in to 0.92 times wcenter) is large relative to those for morpho logy and pumping may be a function of gen- other sponges. This is likely the result of the much der differences within the population (Reiswig 1974). McMurray et al.: Pumping rates of Xestospongia muta 11

X. muta is dioecious and reproduces sexually during ambient currents. This is consistent with the calcula- mass spawning events (Ritson-Williams et al. 2005). tions of Leys et al. (2011) that indicate hydraulic While the relationship between morphology and resistance would be too great for passive flow to gender of X. muta remains to be investigated, anec- occur in species such as X. muta that have thick walls dotal observations during spawning events suggest and relatively long and narrow water canals (Weisz that males may have more cylindrical chimney-like et al. 2008). morphologies, while females may have more bowl-like Near or total pumping cessation was also observed morphologies with v-shaped oscula (S. E. McMurray for approximately 21% of the sponges measured. pers. obs.). Cessation was asynchronous and occurred over inter - Mean excurrent velocities scaled linearly with the vals ranging from 10 to 230 min. Because no more ratio of Vsponge to Aosc, suggesting that volume flow is than 1 cessation event was observed for a given isometric with sponge size; however, there was large sponge over measurement intervals of up to 2.5 d, it variation in w– . Some of this variation was explained was not possible to determine the periodicity of ces- by considering spongocoel morphology. Calculation sation. Pumping cessation is a common characteristic of w– over longer temporal scales further increased among sponges (Reiswig 1971, Vogel 1977, Pile et the variation explained by sponge size and spongo- al. 1997) and typically occurs as a result of reduced coel morphology, suggesting that variation in w– is choanocyte activity or contraction of excurrent canals partly due to temporal changes in pumping activity at the spongocoel (Reiswig 1971). X. muta has a rela- by sponges. Variation in w– may also be due to dif - tively incompressible skeletal architecture and no ferences in the proportion of choanocyte chambers apparent contractions of individuals were observed, between sponges, as was found between male and suggesting that pumping depression is due to a re - females for the sponge V. reiswigi (Reiswig 1974). duction in the activity of choanocytes. Patterns of ces- The diameter of internal aquiferous canals of the sation by X. muta are similar to patterns reported for intertidal sponge Halichondria panacea was found to the sponges T. crypta and V. reiswigi on Jamaican decrease in response to high wave force (Palumbi reefs (Reiswig 1971) and A. fistularis in Barbados 1986). Changes in w– would be expected to be con- (Reiswig 1981). For each species, cessation was asyn- comitant with such changes, but it is unknown whether chronous within the population, uncorrelated with the aquiferous system architecture of X. muta varies changes in the environment, and intrinsically gener- with gradients of hydrodynamic stress on coral reefs. ated. Cessation occurred irregularly for individuals of V. reiswigi and lasted 42 min on average, but occurred at regular intervals of 9 to 21 d for individu- Temporal variation in pumping als of T. crypta and lasted 1 to 5 d. Pumping cessation was found for 13% of the population of A. fistularis Long-term measurements indicated that pumping surveyed (Reiswig 1981). The temporal variations in activity was relatively constant over short temporal pumping reported here support Reiswig’s (1971) scales, but generally varied with the tides. A number hypothesis that thick-walled species working at high of abiotic factors have been shown to effect sponge pressures are unable to maintain constant levels of pumping activity, including turbidity, sedimentation, pumping over time. and temperature (Reiswig 1971, Riisgård et al. 1993). X. muta hosts a diversity of microbes, including Environmental variables varied with the tides, but some that perform a variety of anaerobic processes correlations between pumping by X. muta and envi- (e.g. denitrification) (Fiore et al. 2013). The sig - ronmental variables were not consistent between nificance of pumping depression and cessation to sponges. The common observance of asynchronous sponge and microbial symbiont biology is not well pumping activity among adjacent sponges further understood, and is clearly ripe for future research. supports the conclusion that pumping is uncorrelated Pumping activity is known to influence oxygen con- to the environment. It may be that pumping was not centrations inside the sponge mesohyl, and anoxia measured over a large enough range of environmental can occur within 15 min of cessation (Hoffmann et change to detect a significant relationship. Although al. 2008, Schläppy et al. 2010). Sponge tissue may it is possible for flow to be passively enhanced through switch from aerobic to anaerobic metabolism during the sponge by pressure gradients between the ostia cessation (Schläppy et al. 2010), however, the oxygen and osculum generated by the Bernoulli effect and requirements of sponges may also be relatively low viscous entrainment (Vogel 1977, 1994), we did not compared to other animals (Mills et al. 2014). Hetero- find any evidence of a relationship between w– and geneity of oxygen concentrations within the mesohyl 12 Aquat Biol 23: 1–13, 2014

may influence the spatial and temporal structure of National Science Foundation grants to C.M.F. (Ocean symbiotic microbial communities (Schläppy et al. 2010) Sciences-0751753) and J.R.P. (Ocean Sciences-1029515, 05504658). We thank the staff of the NOAA’s Aquarius Reef and may explain the complexity of microbial pro- Base in Key Largo, Florida, and the crews of the R/Vs ‘Wal- cesses found to occur in X. muta (Fiore et al. 2013). ton Smith’ and ‘Seward Johnson’ for logistical support. Similar to other HMA species with variable pump- Assistance in the field was provided by Kristen Jabanoski, ing activities (Reiswig 1971, 1981), we hypothesize Tiffany Lewis, and Dr. Susanna López-Legentil. Dr. John Carroll provided thoughtful comments on previous versions that pumping variation by X. muta is largely intrinsic of the manuscript. Research in the Florida Keys National over relatively constant environmental conditions; Marine Sanctuary was performed under permit FKNMS- however, the adaptive significance of changes in 2009-126-A1. pumping activity is not apparent. The energetic cost of pumping has long been thought to be low, at LITERATURE CITED approximately 1% of total metabolism (Riisgård et al. 1993); however, recent work suggests that metabolic Bak RPM, Joenje M, de Jong I, Lambrechts DYM, Nieuw- costs may actually be much higher (25 to 28% of total land G (1998) Bacterial suspension feeding by coral reef metabolism) than previous estimates (Hadas et al. benthic organisms. Mar Ecol Prog Ser 175: 285−288 Bell JJ, Davy SK, Jones T, Taylor MW, Webster NS (2013) 2008, Leys et al. 2011). If the energetic cost of pump- Could some coral reefs become sponge reefs as our ing by X. muta is indeed high, then changes in climate changes? Glob Change Biol 19: 2613−2624 pumping activity may be an adaptive response to the Bertin M, Callahan M (2008) Distribution, abundance and availability of picoplanktonic prey (Leys et al. 2011). volume of Xestospongia muta at selected sites in the Reiswig (1971) similarly hypothesized that reduced Florida Keys National Marine Sanctuary. Proc 11th Int Coral Reef Symp 2: 686−690 pumping by the sponge T. crypta at night was in Bidder GP (1923) The relation of the form of a sponge to its response to a reduction of ambient currents and food currents. Q J Microsc Sci 67:293−323 availability. Pumping cessation by X. muta was found Box GEP, Jenkins GM, Reinsel GC (1994) Time series to typically occur at night; however, there was no analysis. Prentice Hall, Upper Saddle River, NJ Cloern J (1982) Does the benthos control phytoplankton bio- clear relationship between ambient currents and mass in south San Francisco Bay? Mar Ecol Prog Ser 9: illumination. 191−202 In conclusion, our results suggest a strong relation- Colvard NB, Edmunds PJ (2011) Decadal-scale changes ship between body size and morphology and sponge in abundance of non-scleractinian invertebrates on a Caribbean coral reef. J Exp Mar Biol Ecol 397: 153−160 pumping rates. Excurrent velocity distributions of X. de Goeij JM, van Oevelen D, Vermeij MJA, Osinga R, muta spanned the spectrum from plug to parabolic- Middelburg JJ, de Goeij AFPM, Admiraal W (2013) like flow, and this variability highlights the careful Surviving in a marine desert: the sponge loop retains characterization of excurrent flow profiles as a pre- resources within coral reefs. Science 342:108−110 requisite to the study of sponge pumping rates. Fur- Díaz MC, Rützler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69: 535−546 ther, we provide a novel hypothesis to explain how Finelli CM, Hart DD, Fonseca DM (1999a) Evaluating the excurrent velocity distributions vary as a function spatial resolution of an acoustic Doppler velocimeter and of the partitioning of sponge biomass relative to the the consequences for measuring near-bed flows. Limnol spongocoel. With the exception of sporadic periods of Oceanogr 44:1793−1801 Finelli CM, Pentcheff ND, Zimmer-Faust RK, Wethey DS cessation, pumping activity was generally constant (1999b) Odor transport in turbulent flows: constraints on over time and uncorrelated with environmental con- animal navigation. Limnol Oceanogr 44:1056−1071 ditions. Importantly, despite variations in sponge mor- Fiore CL, Baker DM, Lesser MP (2013) Nitrogen biogeo- phology and temporal variations in pumping activity, chemistry in the Caribbean sponge, Xestospongia muta: A source or sink of dissolved inorganic nitrogen? PLoS pumping rates were largely proportional to sponge ONE 8: e72961 biomass and can be predicted from simple measure- Gili JM, Coma R (1998) Benthic suspension feeders: their ments of sponge size that are regularly obtained by paramount role in littoral marine food webs. Trends Ecol current coral reef monitoring efforts. Given its large Evol 13: 316−321 biomass and abundance, populations of X. muta González-Rivero M, Yakob L, Mumby PJ (2011) The role of sponge competition on coral reef alternative steady process large volumes of seawater and are predicted states. Ecol Modell 222:1847−1853 to have a dominant influence on water column pro- Hadas E, Ilan M, Shpigel M (2008) Oxygen consumption by cesses on Caribbean coral reefs. a coral reef sponge. J Exp Biol 211: 2185−2190 Hoffmann F, Roy H, Bayer K, Hentschel U, Pfannkuchen M, Brümmer F, de Beer D (2008) Oxygen dynamics and Acknowledgements. This study was funded by a grant from transport in the Mediterranean sponge Aplysina aero- the National Oceanic and Atmospheric Administration’s phoba. Mar Biol 153: 1257−1264 National Undersea Research Program at UNCW and by Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS and McMurray et al.: Pumping rates of Xestospongia muta 13

others (2007) Coral reefs under rapid climate change and Pile AJ, Patterson MR, Witman JD (1996) In situ grazing on ocean acidification. Science 318: 1737−1742 plankton <10 μm by the boreal sponge Mycale lingua. Larsen PS, Riisgård HU (1994) The sponge pump. J Theor Mar Ecol Prog Ser 141:95−102 Biol 168: 53−63 Pile AJ, Patterson MR, Savarese M, Chernykh VI, Fialkov Lewis TB, Finelli CM (2014) Epizoic zoanthids reduce VA (1997) Trophic effects of sponge feeding within Lake pumping in two Caribbean vase sponges. Coral Reefs, Baikal’s littoral zone. 2. Sponge abundance, diet, feeding doi: 10.1007/s00338-014-1226-2 efficiency, and carbon flux. Limnol Oceanogr 42:178−184 Leys SP, Yahel G, Reidenbach MA, Tunnicliffe V, Shavit U, Reiswig HM (1971) In situ pumping activities of tropical Reiswig HM (2011) The sponge pump: the role of current Demospongiae. Mar Biol 9: 38−50 induced flow in the design of the sponge body plan. PLoS Reiswig HM (1974) Water transport, respiration and ener- ONE 6: e27787 getics of three tropical marine sponges. J Exp Mar Biol Loh TL, Pawlik JR (2014) Chemical defenses and resource Ecol 14: 231−249 trade-offs structure sponge communities on Caribbean Reiswig HM (1975) The aquiferous systems of three marine coral reefs. Proc Natl Acad Sci USA 111: 4151−4156 Demospongiae. J Morphol 145:493−502 López-Legentil S, Pawlik JR (2009) Genetic structure of the Reiswig HM (1981) Partial carbon and energy budgets of the Caribbean giant barrel sponge Xestospongia muta using bacteriosponge Verongia fistularis (Porifera: Demospon- the I3-M11 partition of COI. Coral Reefs 28: 157−165 giae) in Barbados. Mar Ecol 2: 273−293 Maldonado M, Ribes M, van Duyl FC (2012) Nutrient fluxes Riisgård HU, Thomassen S, Jakobsen H, Weeks JM, Larsen through sponges: biology, budgets and ecological impli- PS (1993) Suspension feeding in marine sponges Hali- cations. In: Becerro MA, Uriz MJ, Maldonado M, Turon X chondria panicea and Haliclona urceolus: effects of tem- (eds) Advances in sponge science: physiology, chemical perature on filtration rate and energy cost of pumping. and microbial diversity. Adv Mar Biol 62: 113−182 Mar Ecol Prog Ser 96: 177−188 Massaro AJ, Weisz JB, Hill MS, Webster NS (2012) Be- Ritson-Williams R, Becerro MA, Paul VJ (2005) Spawning of havioral and morphological changes caused by thermal the giant barrel sponge Xestospongia muta in Belize. stress in the Great Barrier Reef sponge Rhopaloeides Coral Reefs 24: 160 odorabile. J Exp Mar Biol Ecol 416-417:55−60 Ruzicka RA, Colella MA, Porter JW, Morrison JM and others McArdle BH (1988) The structural relationship: regression (2013) Temporal changes in benthic assemblages on in biology. Can J Zool 66: 2329−2339 Florida Keys reefs 11 years after the 1997/1998 El Niño. McMurray SE, Blum JE, Pawlik JR (2008) Redwood of the Mar Ecol Prog Ser 489:125−141 reef: growth and age of the giant barrel sponge Xesto- Savarese M, Patterson MR, Chernykh VI, Fialkov VA (1997) spongia muta in the Florida Keys. Mar Biol 155: 159−171 Trophic effects of sponge feeding within Lake Baikal’s McMurray SE, Henkel TP, Pawlik JR (2010) Demographics of littoral zone. 1. In situ pumping rates. Limnol Oceanogr increasing populations of the giant barrel sponge Xesto- 42: 171−178 spongia muta in the Florida Keys. Ecology 91: 560−570 Schläppy ML, Weber M, Mendola D, Hoffmann F, de Beer D McMurray SE, Blum JE, Leichter JJ, Pawlik JR (2011) (2010) Heterogeneous oxygenation resulting from active Bleaching of the giant barrel sponge Xestospongia muta and passive flow in two Mediterranean sponges, Dysidea in the Florida Keys. Limnol Oceanogr 56: 2243−2250 avara and Chondrosia reniformis. Limnol Oceanogr 55: Meroz-Fine E, Shefer S, Ilan M (2005) Changes in morpho - 1289−1300 logy and physiology of an East Mediterranean sponge in Southwell MW, Weisz JB, Martens CS, Lindquist N (2008) In different habitats. Mar Biol 147: 243−250 situ fluxes of dissolved inorganic nitrogen from the Mills DB, Ward LM, Jones C, Sweeten B, Forth M, Treusch sponge community on Conch Reef, Key Largo, Florida. AH, Canfield DE (2014) Oxygen requirements of the Limnol Oceanogr 53: 986−996 earliest animals. Proc Natl Acad Sci USA 111:4168−4172 Vermeij GJ (1993) Evolution and escalation: an ecological Monismith SG, Davis KA, Shellenbarger GG, Hench JL and history of life. Princeton University Press, Princeton, NJ others (2010) Flow effects on benthic grazing on phyto- Vogel S (1977) Current-induced flow through living sponges plankton by a Caribbean reef. Limnol Oceanogr 55: in nature. Proc Natl Acad Sci USA 74: 2069−2071 1881−1892 Vogel S (1994) Life in moving fluids. Princeton University NOAA (National Oceanic and Atmospheric Administration) Press, Princeton, NJ (2007) Florida Keys National Marine Sanctuary revised Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bi - management plan. US Department of Commerce, NOAA, variate line-fitting methods for allometry. Biol Rev Camb National Ocean Service, Silver Spring, MD Philos Soc 81:259−291 Officer CB, Smayda TJ, Mann R (1982) Benthic filter feed- Weisz JB, Lindquist N, Martens CS (2008) Do associated ing: a natural eutrophication control. Mar Ecol Prog Ser micro bial abundances impact marine demosponge pump- 9: 203−210 ing rates and tissue densities? Oecologia 155: 367−376 Palumbi SR (1986) How body plans limit acclimation: re - Yahel G, Post AF, Fabricius K, Marie D, Vaulot D, Genin A sponses of a demosponge to wave force. Ecology 67: (1998) Phytoplankton distribution and grazing near coral 208−214 reefs. Limnol Oceanogr 43: 551−563 Peterson BJ, Chester CM, Jochem FJ, Fourqurean JW (2006) Yahel G, Sharp JH, Marie D, Häse C, Genin A (2003) In situ Potential role of sponge communities in controlling feeding and element removal in the symbiont-bearing phytoplankton blooms in Florida Bay. Mar Ecol Prog Ser sponge Theonella swinhoei: bulk DOC is the major 328: 93−103 source for carbon. Limnol Oceanogr 48: 141−149

Editorial responsibility: Josep-Maria Gili, Submitted: July 10, 2014; Accepted: October 26, 2014 Barcelona, Spain Proofs received from author(s): November 24, 2014