The influence of flow velocity and food concentration on Lophelia pertusa (Scleractinia) zooplankton capture rates

Journal of Experimental Marine Biology and Ecology 395 (2010) 55–62

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Journal of Experimental Marine Biology and Ecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j e m b e

The influence of flow velocity and food concentration on Lophelia pertusa (Scleractinia) zooplankton capture rates Autun Purser a,⁎, Ann I. Larsson b, Laurenz Thomsen a, Dick van Oevelen c a b c

Jacobs University, Campus Ring 1, 28759 Bremen, Germany Department of Marine Ecology, University of Gothenburg, Tjärnö, SE-452 96 Strömstad, Sweden Centre for Estuarine and Marine Ecology, Netherlands Institute of Ecology (NIOO-KNAW), POB 140, 4400 AC Yerseke, The Netherlands

a r t i c l e

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Article history: Received 6 February 2010 Received in revised form 2 August 2010 Accepted 6 August 2010 Keywords: Carbon storage Cold-water coral Feeding rate Flume Lophelia pertusa

a b s t r a c t Lophelia pertusa is the most significant framework building scleractinian coral in European seas, yet the reproductive strategy, longevity, growth and food capture rates for the species remain poorly understood. In this study an experimental investigation into the ability of L. pertusa to capture zooplankton from suspension was conducted. By direct ROV sampling approximately 350 L. pertusa polyps were collected from the Tisler reef, Norway and maintained under temperature controlled conditions in recirculating flumes. These polyps were subdivided into three replicate groups of ~120 polyps and maintained in waters with flow velocities of 2.5 cm s− 1 or 5.0 cm s− 1. Suspended Artemia salina nauplii food concentrations of between 345 and 1035 A. salina l− 1 were introduced. L. pertusa net capture rates were assessed by monitoring the reduction in suspended A. salina concentration in each flume over 24 h. Maximum net capture rates were higher in flumes with a 2.5 cm s− 1 flow regime, at 73.3± 2.0 A. salina polyp− 1 h− 1 (mean± SD) than those with 5 cm s− 1 flow (19.8± 11.8 A. salina polyp− 1 h− 1). Maximum net capture rates were lower in flumes with A. salina densities of b 690 A. salina l− 1 than in flumes with higher food densities under comparable flow velocities. The maximum net capture rates observed represent maximum carbon capture rates of 66.4± 2.0 μg C polyp− 1 h− 1 and 17.9± 10.7 μg C polyp− 1 h− 1 under 2.5 and 5 cm− 1 s− 1 flow speeds respectively. The results of this study indicate that L. pertusa captures zooplankton more efficiently under slower flow velocities. © 2010 Elsevier B.V. All rights reserved.

1. Introduction The scleractinian coral Lophelia pertusa (Linneaus, 1758) is one of the most widespread of the reef building cold-water coral (CWC) species (Roberts et al., 2009). Unlike many tropical or warm water scleractinian corals, L. pertusa is azooxanthellate, not living in association with algal symbionts (Rogers, 1999; Freiwald et al., 2004). This lack of an algal symbiont allows for a species distribution outside of the photic zone (Zibrowius, 1989). L. pertusa forms bushy calcium carbonate colonies with growth, with a thin surface layer of living polyps growing on top of the dead skeletal material secreted by previous generations (Riding, 2002). The growth rate of L. pertusa has been observed to be a moderate 6–25 mm per year in most natural environments, with individual polyps attaining maximum dimensions of roughly 1 cm diameter and several cm length (Mikkelsen et al., 1982; Mortensen and Rapp, 1998; Orejas et al., 2008; Roberts et al., 2009). Extensive reefs have been found in many regions of the world ocean (Wilson, 1979; Roberts et al., 2006), often forming structures meters in height and km2 in coverage area (De Mol et al., 2002). Such

⁎ Corresponding author. Tel.: + 49 421 200 5865. E-mail address: [email protected] (A. Purser). 0022-0981/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2010.08.013

sizes imply reef longevities in the order of 100 to 1000 ky (Freiwald et al., 1999). The volume of these calcium carbonate structures may render L. pertusa reefs significant long-term carbon storage reservoirs (van Weering et al., 2003; Noé et al., 2006). A host of environmental factors influence reef distribution, with food availability and suitability of substrate being of paramount importance (Davies et al., 2008). Lophelia pertusa reefs are often associated with regions of the seabed exposed to elevated current velocities, such as seamounts and carbonate mounds (Dorschel et al., 2005; Huvenne et al., 2007), shelf margins (Fosså et al., 2002) or sills (Jonsson et al., 2004). At many of these sites however, periods with reduced flow velocities have been observed, often associated with tides (Davies et al., 2009). It has been proposed that Lophelia pertusa reefs are hotspots of biodiversity (Henry and Roberts, 2007) and carbon cycling on continental margins (Van Oevelen et al., 2009). The dead skeletal reef material provides a varied habitat for both sessile and mobile benthic organisms (Mortensen et al., 1995). The complex reef structure can greatly influence the local hydrodynamics in the reef vicinity, providing further diversity in habitat niches (Dorschel et al., 2007; Roberts et al., 2008). It has been hypothesised that these variegated reef structures may provide refuge for juvenile fish of commercial species (Costello et al., 2005). This hypothesis is particularly prescient on the Norwegian Margin where L. pertusa

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A. Purser et al. / Journal of Experimental Marine Biology and Ecology 395 (2010) 55–62

reefs are well-developed (Mortensen et al., 2001) and where fishery activity is high (Fosså et al., 2002; Hall-Spencer et al., 2009). This is also a region where the offshore hydrocarbon industry is in operation and public/governmental concern over the potential impact of this industry on reef ecosystems is high (Lepland and Mortensen, 2008). In Norway, and progressively elsewhere in European waters, this concern has led to protective legislation being put in place soon after reefs are discovered. Examples of such legislation being the instigation of fishing exclusion zones and the requirement for detailed oceanographic and benthic surveys prior to granting of oil and gas exploration licenses across the Norwegian Margin (Davies et al., 2007; Fosså and Skjoldal, 2010). The diet of Lophelia pertusa has been investigated previously by analysing stable isotope ratios (Duineveld et al., 2004) bulk fatty acid composition (Kiriakoulakis et al., 2005) and lipids (Dodds et al., 2009) of polyp samples collected from reefs in the northeast Atlantic. These direct analyses indicate that the diet of L. pertusa varies from site to site, and that the organism may be generally heterotrophic, taking whatever is available from the water column, as has been observed in other scleractinian corals (Sebens et al., 1996; Rosenfeld et al., 2003; Houlbreque et al., 2004; Van Oevelen et al., 2009). Samples collected with sediment traps or in-situ pumps have shown a great variety both temporally and spatially in the quality of organic material entering L. pertusa reef environments (Kiriakoulakis et al., 2007). Although there have been experimental investigations of food capture rates carried out with tropical scleractinian corals, gorgonians (Coles, 1969; Sebens and Johnson, 1991; Sebens et al., 1996; Ferrier-Pagès et al., 2003; Hii et al., 2009) and other anthozoans (Anthony, 1997) few have been conducted with scleractinian cold-water corals (Tsounis et al., 2010). The objective of this study was to investigate in the laboratory whether net capture rates by Lophelia pertusa of live zooplankton (Artemia salina) is influenced by flow velocity or available A. salina food concentration. Two hypotheses were investigated. Firstly, that the net capture rate by Lophelia pertusa increases with increasing flow velocity, and secondly, that net capture rates are higher when available food concentration is higher. 2. Materials and methods

from trawl-displaced coral blocks originating in a less pristine section of the reef (58° 59.695 N; 10° 58.240 E). Coral branches were sampled in fragments each containing between 10 and 50 polyps from a number of displaced coral blocks. These fragments were placed in a collection drawer on the ROV for return to the surface. On deck they were transferred into a large coolbox filled with 8 °C bottom water and transported to the University of Gothenburg field station at Tjärnö. The total transport time from seabed to field station was less than 2 h. 2.2. Lophelia pertusa preparation At the Tjärnö field centre the Lophelia pertusa fragments were transferred to a thermoconstant laboratory room maintained at 8 °C. The fragments were then further divided manually by cracking with latex-gloved fingers into 45 branches, each consisting of between 5 and 25 live polyps. Each of these branches was then photographed using a Fujifilm E900 9.0 megapixel digital camera and placed on a plastic grid in one of three flow-through 25 l plastic aquaria. Seawater supplied to each aquarium was pumped from 45 m depth in the adjacent Koster fjord. Salinity varied from 32 to 34 and temperature was maintained at 8 °C. Each aquarium was delivered sand-filtered seawater direct from the Kosterfjord from a depth of 45 m at a rate of ~ 2 l min− 1. The coral branches were maintained under these conditions for three weeks prior to the commencement of the experimental investigations and provided with a daily dose of ~ 0.5 g freshly hatched Artemia salina nauplii delivered to each aquarium. The intention of providing a uniform food supply to the experimental aquaria prior to conducting the experimental runs was to ideally equalize the polyps response to the experimental food concentrations, as branch orientation prior to collection could have influenced recent feeding history of individual polyps. The Sven Loven Centre has maintained L. pertusa successfully for a number of years under these flow and feeding regimes. Each Lophelia pertusa fragment was numbered and number of living polyps counted. The diameter of each living polyp cup was determined by analysing the photographs using a PC and the ImageJ 1.42q software application.

2.1. Lophelia pertusa collection site and sampling method 2.3. Flume setup The live coral fragments used in this study were collected from the Tisler reef in the Norwegian section of the Skagerrak, several km north of the Swedish border. First surveyed in 2002 (Lavaleye et al., 2009), the reef forms an elongated structure ~ 1200 m by ~200 m on a sill between the Tisler islands and the Norwegian mainland, in water depths of 70–155 m. Clearly damaged by heavy trawl activity, a trawl ban was put in place at the reef in 2003(Fosså and Skjoldal, 2010). The reef is made up of a large number of ~ 2 m diameter, ~1 m high Lophelia pertusa thickets surrounded by fields of coral rubble (Purser et al., 2009). In some areas the thickets have merged into larger horizontal structures but there is little of the vertical growth apparent at some L. pertusa reefs, such as those on the Norwegian continental margin (Mortensen et al., 2001; Freiwald et al., 2002) or the Porcupine Seabight (Huvenne et al., 2007). Free stream velocities over the sill can vary between 0.0 and 40.0 cm s− 1 throughout the year, with direction of flow fluctuating irregularly between NW and SE (Lavaleye et al., 2009). The composition of particulate material entering the Tisler reef has been investigated in several studies (Kiriakoulakis et al., 2005) and in-situ pump collections have shown periodically high concentrations of fresh phytoplankton and zooplankton swimmers within the bottom waters at the site during spring and summer (Lavaleye et al., 2009). Due to the sensitivity of the ecosystem selective sampling was carried out using the specially modified arm of a Sperre SubFighter 7500 DC ROV in July 2008. Approximately 350 polyps were collected

Three replicate recirculating flumes (Fig. 1) were set up in an 8 °C thermoconstant room. Each flume was of 58 l volume and constructed primarily out of plexiglass, with a plastic return pipe fitted with a motor driven propeller to maintain recirculation (Berntsson et al., 2004). The motor driven propeller in each flume was capable of maintaining a constant flow of up to 7 cm s− 1. The 45 coral branches were randomized into three sets of 15. These sets were each fixed to the acrylic bases of the flume test sections by inserting the branch bases into a 1 cm silicone hose section glued to the flume base. Five branches were mounted in each of three equally

Fig. 1. Scale diagram of recirculating plexiglass flume setup. For all experimental runs, three identical flumes were maintained. a) Coral branches in plastic mount. b) Direction of circulation. c) Artemia salina delivery point and location of sampling for A. salina concentration determination. d) Motor. e) Opaque plastic return pipe.

A. Purser et al. / Journal of Experimental Marine Biology and Ecology 395 (2010) 55–62

spaced rows perpendicular to the direction of flow in each flume. Each coral row was positioned 4 cm apart. 2.4. Food characterisation Freshly hatched Artemia salina nauplii were used in the experimental runs. A. salina are a standard food source used in coral cultivation in the laboratory (Coles, 1969; Lasker, 1981; Dai and Lin, 1993; Houlbreque et al., 2004). New cysts were hatched under standard conditions in an incubation aquarium. Following hatching, the concentration of Artemia salina was determined by taking five 1 ml subsamples from the incubation aquaria and filtering onto 0.45 μm filter papers. The number of A. salina on each filter paper was counted under a dissecting microscope at 25× magnification, with the mean taken from the five subsamples. From this average the volume of water from the incubation chamber required to deliver a known quantity of A. salina to each of the experimental flumes could be determined. To assess the C and N concentrations within freshly hatched nauplii triplicate 0.2 ml samples of freshly hatched A. salina were taken on two hatching days. The number of A. salina in the 0.2 ml samples was counted on a glass slide under a dissecting microscope prior to analysis for total C and total N in an element analyser (EURO EA) after the method in Pike and Moran (1997). 2.5. Experimental runs After transfer to the recirculating flumes, the coral fragments were maintained in the dark at 8 °C for a week under a constant flow of 2.5 cm s− 1 to allow for acclimatisation. Every 24 h during this period the water in each flume was replaced with fresh seawater pumped directly from the Kosterfjord by simultaneously siphoning out the old water and piping in new water. To ensure a significant changeover, this process was conducted for 30 min in each flume with an inflow of ~ 3 l min− 1 being maintained. During this acclimatisation week a moderate quantity of Artemia salina was delivered to each flume on day 5. Any food remaining after 24 h was removed by the siphoning process and additional filtering. Following the acclimatisation period the experimental runs commenced. Experimental runs were conducted at 2.5 and 5 cm s− 1 flow velocities, with Artemia salina densities of 345, 690, and 1035 A. salina l− 1. Experimental runs of each flow velocity and food concentration combination were conducted once in each of the experimental flumes (giving n = 3 for each 2 factor treatment). Coral branches in each flume were not randomized between each experimental run, but maintained in the same flumes throughout the experimental period. This was to reduce the potential stress impact of handling on the capture rate results. The order of experiments, however, was randomized by both flow speed and initial A. salina l− 1 concentration. The Artemia salina food supply was delivered by large syringe directly into the flume water at 2 cm depth near the start of the flume return section (Fig. 1). Following delivery, A. salina concentrations in suspension were monitored over a 24 h period. Monitoring was conducted by taking triplicate subsamples of ~100 ml volume periodically from each flume (~2–8 h between samples). The behaviour of the Lophelia pertusa polyps was also observed qualitatively at the time of each sampling, with polyps being classified as ‘extended fully’, ‘swept

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back with flow’ or ‘retracted’. The triplicate samples were taken by siphoning out water directly from the same depth and location as food was introduced to the flume. A 1 cm diameter silicone hose was used for extraction with the open end facing into direction of flow. Each subsample was filtered onto a 0.45 μm filter paper and the number of A. salina counted under a dissecting microscope. Concentrations from the subsamples were plotted and an equation for the best fit line determined. From these best fit equations the average net capture rate flume h− 1 was determined, based on the reduction over 24 h in suspended Artemia l− 1 concentration. This figure was divided by polyps flume− 1 to determine the average net capture rate polyp− 1 h− 1. The maximum net capture rate h− 1 for each flume derived similarly, but based on the concentration reduction over the first 6 h of each experimental run. These capture rates represent the average and maximum number of A. salina removed from suspension polyp− 1 h− 1 rather than the number ingested by each polyp. This study did not attempt to determine the number of A. salina entrapped in coral mucus, deposited on the floor of the flume, trapped within the coral structure or consumed by the living polyps. They reflect the removal from suspension and delivery to the reef ecosystem (flume floor and coral structure) of suspended zooplankton. After each 24 h experimental run the water in each flume was replaced with new piped seawater over a 30 min period (see Section 2.2). A 63 μm sieve was then placed in each flume at the sampling position for 3 h to catch any remaining suspended Artemia salina. Each flume was then left undisturbed but under constant flow (the flow speed as used in the previous experimental run) for 21 h prior to commencement of the next experimental run. Following completion of the experimental runs, the total buoyant weight, number of polyps and polyp diameters were determined for coral fragments in each flume (Table 1). Buoyant weight of the coral fragments was determined as described in Davies (1989), in seawater of 8 °C and salinity of 33. 2.6. Control runs To ensure that the average and maximum net capture rates observed during experimental runs was not purely the result of the Artemia salina either becoming stuck within the coral structure or trapped within the flumes, control runs were conducted following the live coral experimental runs. For these runs, 15 dead coral fragments of comparable size to those used in the live experimental runs were placed in each flume in the same plastic mounts as used previously. Control runs were conducted with flow velocities of both 2.5 and 5.0 cm s− 1, with 1035 A. salina l− 1 nauplii density. The A. salina concentration within each flume was monitored over 24 h as during the live experimental runs (see Section 2.5). 2.7. Statistical analysis The correlation between maximum net capture rates and changes in food density and flow speed was analysed with a two-way repeated measures ANOVA across the three experimental flumes. Data transformation was not necessary as as Mauchley's test found the variances in the differences between conditions to be non-significant (Mauchley, 1940). Where significant differences were indicated between factor levels, a Holm–Sidak post-hoc multiple comparison

Table 1 Table showing the number of live Lophelia pertusa polyps, the average polyp diameter and buoyant weights of all branches used in each of the experimental flumes. Flume

Polyp no.

Buoyant weight (g)

Total feeding area (mm2)

Mean polyp area (mm2)/SD

Mean polyp dia. (mm)/SD

Median dia. (mm)

Mode dia. (mm)

A B C

128 115 116

45 42 36

4338 3398 3539

37.5/11.3 33.5/12.2 34.8/20.6

6.50 ± 1.05 6.16 ± 1.28 5.87 ± 1.34

6.0 6.0 5.0

7.0 7.0 7.0

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test was used to determine between which levels the difference was significant. Whether variation in observed net capture rates over 24 h correlated with different initial food concentrations or flow speeds was investigated by using a two-way repeated measures ANOVA. As with maximum net capture rates, Mauchley's test found no significant differences in variances in the dataset, so data transformation was not required prior to analysis. As with analysis of the maximum net capture rates, A Holm–Sidak post-hoc test was used where appropriate. Maximum net capture rates observed in the control runs were compared with those observed in the experimental runs. A two-way repeated measures ANOVA with flow speed (2.5 and 5.0 cm s− 1) and coral condition (dead or alive) as independent variables, the repeated measures design was employed to allow for any flume effect. Initial food concentrations of 1035 Artemia l − 1 were used in this comparison. 3. Results 3.1. C and N concentrations of Artemia salina nauplii Total C concentration found within each freshly hatched Artemia salina nauplii was 0.905 μg C A. salina nauplii− 1 (SD=1.614×10− 2). Total N concentration was 0.175 μg N A. salina nauplii− 1 (SD=3.696×10− 3). 3.2. Coral condition, flow velocity and maximum net capture rates Maximum net capture rates in flumes containing living coral fragments with an initial food availability concentration of 1035 Artemia l− 1 varied with flow velocity. Under 2.5 cm s− 1 flow the maximum net capture rate was 73.3 ± 2.0 Artemia polyp− 1 h− 1. Under 5.0 cm s− 1 flow a lower maximum net capture rate of 19.8 ± 11.8 Artemia polyp− 1 h− 1 was observed. When these runs were repeated with dead coral fragments in the flumes maximum net capture rates were lower. Under 2.5 cm s− 1 maximum net capture was 6.1 ± 12.2 Artemia polyp− 1 h− 1, and under 5.0 cm s− 1 flow, the rate was higher at 10.2 ± 9.35 Artemia polyp− 1 h− 1. Flow speed had a statistically significant effect on maximum net capture rates when comparing living and dead coral fragments under the two flow speeds tested (F = 100.90, p = 0.01). Coral health (living or dead) also significantly affected maximum net capture rates (F = 38.21, p b 0.05). The interaction of flow speed and coral health had a strong influence on maximum net capture rates (F = 158.17, p b 0.01), reflecting the fact that for live corals, increasing flow speed reduced maximum net capture rates, whereas in runs with dead corals, increasing flow speed increased maximum net capture rates.

Fig. 2. Mean maximum net capture rate of Artemia salina polyp− 1 h− 1. White bars represent maximum net capture rates under 2.5 cm s− 1 flow. Black bars represent maximum net capture rates under 5.0 cm s− 1 flow. Error bars represent 1 SD (N = 3 for each treatment).

net capture rate with an initial food concentration of 345 Artemia l− 1 was 8.7±1.8 Artemia polyp− 1 h− 1. Increasing the initial food concentration of 690 Artemia l− 1 also increased the maximum net capture rate to 20.2±9.5 Artemia polyp− 1 h− 1. A further increase of the initial food concentration to 1035 Artemia l− 1 did not result in a further increase in maximum net capture rate, with a rate of 19.8± 11.8 Artemia polyp− 1 h− 1 being recorded. Under 5.0 cm s− 1 flow, standard deviation was lowest at 345 Artemia l− 1 initial food concentration (SD=1.8), with both runs of higher initial food concentrations having standard deviations ~6× greater. Statistically, both flow speed (F = 80.376, p b 0.05) and initial food concentration (F = 62.322, p b 0.01) had an effect on maximum net capture rates. For initial food concentrations, A Holm–Sidak post-hoc multiple comparison test showed the significant differences in these capture rates to be between 345 Artemia l− 1 and both higher concentrations, initial concentrations. There was no statistical interaction between the effects of flow speed and initial food concentration. 3.4. The effect of flow speed on average net capture rates under different initial food concentrations Average net capture rates were higher under 2.5 cm s− 1 flow than under 5.0 cm s− 1 flow conditions (Fig. 3), with average net capture rates also being influenced by initial food concentration. Under 2.5 cm s− 1 flow, the change in Artemia l− 1 in suspension did not decrease linearly over time in any of the runs carried out with live

3.3. The effect of flow speed on maximum net capture rates under different initial food concentrations Throughout experimental runs at both flow velocities, Lophelia pertusa polyps were generally observed to have their tentacles swept back with the flow of water. Under 5.0 m s− 1 flow, tentacles were swept further back than under a flow of 2.5 cm s− 1. Maximum net capture rates were greater under 2.5 cm s− 1 than 5.0 cm s− 1 flow velocity (Fig. 2). The effect of flow velocity on maximum net capture rates was also dependant on food concentration. Under a 2.5 cm s− 1 flow regime, maximum net capture rates scaled with initial food concentration. The lowest maximum net capture rate observed under these flow conditions was 26.8±17.4 Artemia polyp− 1 h− 1 with an initial food concentration of 345 Artemia l− 1. With an initial food concentration of 690 Artemia l− 1, the maximum net capture rate was higher at 57.7±5.7 Artemia polyp− 1 h− 1. At the higher initial food concentration of 1035 Artemia l− 1 the maximum net capture rate was 73.3±2.0 Artemia polyp− 1 h− 1. Under 2.5 cm s− 1 flow, standard deviation in maximum capture rates decreased with increasing initial food availability. Under 5.0 cm s− 1 flow, the maximum

Fig. 3. Mean average net capture rate of Artemia salina polyp− 1 h− 1. White bars represent average net capture rates under 2.5 cm s− 1 flow. Black bars represent average net capture rates under 5.0 cm s− 1 flow. Error bars represent 1 SD (N = 3 for each treatment).

A. Purser et al. / Journal of Experimental Marine Biology and Ecology 395 (2010) 55–62

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Fig. 4. Artemia salina concentration over time under 2.5 cm s− 1 flow in flume C. R2 values for best fit lines N 0.8. Error bars represent 1 SD (N = 3 for each treatment).

coral. Under 2.5 cm s− 1 flow velocity, the reduction in Artemia l− 1 over time was best modelled by logarithmic trend lines (Fig. 4). The reduction in concentration was greater during the first ~ 4 h in all the live experimental runs, indicating a higher net capture during this initial period of food availability. The average net capture rate with an initial food concentration of 345 Artemia l− 1 under 2.5 cm s− 1 flow was 6.19 ± 1.21 Artemia polyp− 1 h− 1. With an initial food availability of 690 Artemia l− 1 the average net capture was approximately double this rate at 13.64 ± 0.49 Artemia polyp− 1 h− 1. With an initial food concentration of 1035 Artemia l− 1 the average net capture was again higher, at 16.15 ± 2.12 Artemia polyp− 1 h− 1. Under 5.0 cm s− 1 flow, Artemia l− 1 concentration decreased at a more uniform rate throughout all experimental runs with live corals than under 2.5 cm s− 1 flow (Fig. 5). The decrease was best modelled by exponential trend lines. Under 5.0 cm s− 1 flow average net capture rate was 5.23± 0.07 Artemia polyp− 1 h− 1 with an initial available food concentration of 345 Artemia l− 1. With an initial food concentration of 690 Artemia l− 1 this rate was roughly doubled to 10.22± 0.06 Artemia polyp− 1 h− 1. Further increasing food concentration had little effect on the average net capture rate under 5.0 cm s− 1 flow, with a rate of 11.36± 0.61 Artemia polyp− 1 h− 1 recorded for 1035 Artemia l− 1 initial food availability. Under both flow velocities, average net capture rates increased with increased initial food availability, but not linearly. Under both flow regimes, each increase in initial food availability had a progressively

less pronounced effect on the increase in the average net capture rate. Standard deviations did not vary greatly between experimental runs, but at both flow velocities standard deviations were greatest in runs containing the highest initial food concentration of 1035 Artemia l− 1. Food concentration had a statistically significant effect on average net capture rates (F = 106.68, p b 0.005). A Holm–Sidak post-hoc multiple comparison test showed that there were significant differences in average net capture rates between runs with initial available food concentrations of 345 Artemia l− 1 and both 690 and 1035 Artemia l− 1 concentrations. No significant difference in average net capture rates between 690 and 1035 Artemia l− 1 concentrations was indicated by the post-hoc test. Statistically, average net capture rates over the 24 h experimental period were not influenced by flow speed. Table 2 shows the average C polyp− 1 h− 1 and total C polyp− 1 day− 1 net capture rates for each experimental run. 4. Discussion 4.1. The influence of flow speed and food concentration on net capture rates Both the maximum net capture and average net capture rates observed in the experimental runs indicate a more efficient capture of

Fig. 5. Artemia salina concentration over time under 5.0 cm s− 1 flow in flume C. R2 values for best fit lines N0.8. Error bars represent 1 SD (N = 3 for each treatment).

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Table 2 Table showing the average Artemia salina net capture rates polyp− 1 h− 1, the average C polyp− 1 h− 1 and C polyp− 1 day− 1 from the experimental and control runs. Flow (cm s− 1)

Initial conc.

Average net capture rate (polyp− 1 h− 1) ± SD

C capture (μg C polyp− 1 h− 1) ± SD

C capture (μg C polyp− 1 day− 1) ± SD

2.5 2.5 2.5 2.5 control 5.0 5.0 5.0 5.0 control

345 690 1035 1035 345 690 1035 1035

6.19 ± 1.21 13.64 ± 0.49 16.15 ± 2.12 3.11 ± 1.68 5.23 ± 0.07 10.22 ± 0.06 11.36 ± 0.61 2.47 ± 1.01

5.60 ± 1.09 12.34 ± 0.44 14.62 ± 1.92 2.81 ± 1.52 4.73 ± 0.06 9.25 ± 0.05 10.28 ± 0.55 2.23 ± 0.91

134.44 ± 26.28 296.26 ± 10.64 350.88 ± 46.05 67.55 ± 36.49 113.59 ± 1.52 221.97 ± 1.30 246.74 ± 13.24 53.65 ± 21.94

zooplankton food by Lophelia pertusa under 2.5 cm s− 1 than 5.0 cm s− 1 flow conditions. This is initially surprising given that to date L. pertusa occurrence has often been associated with regions with high bottom current velocities (Messing et al., 1990; Thiem et al., 2006; White, 2007). Recent in-situ studies have indicated that at some reef sites, such as the Mingulay reef (Davies et al., 2009) the strong prevalent currents are reduced in velocity for a period of a few hours during each tidal cycle. Flow velocities measured from the vicinity of cold-water coral reefs are often reported from several meters above the seabed, and the boundary effect may render currents at the coral interface weaker. Additionally, within the complex 3D structure of a natural L. pertusa reef there are likely to be many areas of further reduced flow, as observed at tropical reefs (Sebens and Johnson, 1991; Sebens et al., 1997). Within some dense coral thickets near stagnant, diffusion dominated regions are likely to develop (Kaandorp et al., 2005), even with a high prevailing regional flow. In Sebens and Johnson (1991), capture rates across such a complex reef structure were investigated at a shallow water reef at Salt River Canyon, St Croix, United States Virgin Isles for the warm water coral Madracis decactis. They report a marked variation in zooplankton capture rates, with net capture rates increasing with flow speed. From this study it would seem that capture of zooplankton (of the 200– 250 μm range) by L. pertusa is more successful under slow flow conditions. There are several possible explanations for the large differences observed in capture rates by L. pertusa under the two flow velocities investigated. Although increasing flow velocity delivers a greater flux of food to corals, increasing the encounter rate (Best, 1988), polyp tentacles may also be progressively swept back with flow, reducing the feeding surface of the polyps. The progressively greater bending of polyp tentacles with increasing flow velocities has been observed in previous studies of soft corals (Fabricius et al., 1995), anemones (Anthony, 1997), gorgonians (Dai and Lin, 1993) and tropical scleractinians (Sebens and Johnson, 1991). Dai and Lin (1993) compared feeding efficiency and polyp deformation under flow for three gorgonian species. They observed that although the tentacles of Subergorgia suberosa polyps would be swept back with flow more readily with increasing flow than Acantogorgia vegae or Melithaea ochracea, S. suberosa would capture food most efficiently at lower flow velocities. They identified optimal feeding flow velocity ranges for the three species, with the optimum ranges correlating with the flow velocities at which the species could maintain their polyp tentacles extended into the flow. A further possible explanation for reduced capture rates at higher velocities is that zooplankton entrapment by the polyps following an encounter may be less successful. Higher flow velocities may give the suspended prey sufficient momentum to break free of entrapping mucus strands or tentacle cilia. Should a polyp capture prey under these higher flow conditions, dislodgement of the zooplankton prior to the coral successfully bringing it to its mouth for consumption could also be more likely, as has been observed in octocorals (Wainwright and Koehl, 1976; Patterson, 1984; McFadden, 1986). Low zooplankton concentrations appear to inhibit maximum and average net capture rates by Lophelia pertusa at both flow velocities used in this study. Maximum net capture rates increased with increased food

availability under 2.5 cm s− 1 flow. Average net capture rates also increased with food availability, but to a lesser extent. From the logarithmic Artemia salina concentration reductions over the 24 h experimental period it appears that L. pertusa polyps capture a required quantity of food as swiftly as possible, and thereafter reduce their capture effort. The total numbers of A. salina captured polyp− 1 day− 1 by L. pertusa were similar for runs with initial concentrations of 690 and 1035 A. salina l− 1, representing a daily C capture of ~280–400 μg C polyp− 1 day− 1. In a recent study by Tsounis et al. (2010) a higher Artemia salina nauplii maximum net capture rate by L. pertusa was reported of 462± 212 μg C polyp− 1 h− 1. In their study, a different methodology was employed with a lower flow rate of 1.0 cm s− 1, and a 10× higher initial Artemia l− 1 concentration. Under 2.5 cm s− 1 flow and 1035 Artemia l− 1 maximum net capture in this study was 73.2±2.0 Artemia polyp− 1 h− 1, equating to 66.25±1.8 μg C polyp− 1 h− 1. Although a more moderate capture rate than that reported by Tsounis et al., it is within an order of magnitude. There are several possible reasons for the discrepancy in findings of the two studies. In the Tsounis et al. study L. pertusa were collected from the Mediterranean for use in the experimental work, and maintained in 12 °C water throughout the experimental period. Dodds et al. (2007) demonstrated that even moderate increases in temperature results in a large increase in Q10 values for oxygen consumption within the species, indicating an increase in metabolic rate and requirement for a larger energy input. The 4 °C temperature difference between the two experiments may account for the larger carbon capture rate observed in the Mediterranean L. pertusa in the Tsounis et al. experiments. A further possible explanation for the difference in net capture could be a more efficient entrapment of A. salina nauplii within coral mucus under the slower flow conditions used in their study. The maximum and average net C capture rates determined in this study do not necessarily equal the number of Artemia salina nauplii successfully consumed by Lophelia pertusa polyps, rather they represent the removal from suspension of the A. salina nauplii by either direct consumption, entrapment within coral surface mucus or by weighting down the nauplii following contact with mucus. In the field such zooplankton would then provide input into the complex reef food web (van Weering et al., 2003), most likely to be consumed and cycled by the suspension and filter-feeding reef associated organisms (Van Oevelen et al., 2009). 4.2. The influence of coral health, reef morphology and polyp age on net capture rates Removal of Artemia salina from suspension was not purely the result of entrapment within the coral structure or loss to the flumes. A slightly higher maximum net capture and average net capture rate were observed during the control runs under 5.0 than 2.5 cm s− 1 flow velocity. This is opposite to what was observed during the runs with live coral fragments. The A. salina nauplii used in this study were unable to swim against flow velocities of even 1 cm s− 1 (pers. obs.) and therefore could be considered analogues for suspended particles and sediments of ~ 200–250 μm. Within this study the variation in fine scale flow within and around the coral fragments was not investigated

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and the magnitude of any wake effect behind the line of coral branches not known. It would appear from these results that increasing flow to L. pertusa structure increases the passive net capture rate of suspended material by the reef environment. However, the overall flux of material to a living reef appears to be reduced under higher flow conditions, as the active net capture rates of L. pertusa appear to decrease more rapidly with flow acceleration than passive capture rates increase. The spacing of Lophelia pertusa branches in this flume study was uniform across the flumes, but was not representative of all natural reef situations. Within the experimental flumes there were gaps between the branches of several cm, as is found at some reef sites, such as the small outcroppings within Mediterranean canyons (Orejas et al., 2009). Larger, more developed reefs such as those on the Norwegian Margin (Freiwald et al., 1997) consist mainly of regions of densely packed, anastomosed coral branches. Sebens et al. (1997) investigated the effect of branch density and flow speed on net capture rates by the shallow water coral Madracis mirabilis. They observed that low branch densities resulted in a higher net capture rate under low flow conditions (up to 5 cm s− 1) than was achieved by high branch densities. Above 5 cm s− 1, they observed net capture rates by low branch densities to fall rapidly, but to increase for high branch densities, peaking at a flow rate of ~ 10 cm s− 1, with a capture rate 2.5× the maximum observed by low branch densities at the lower flow velocities. They hypothesised that the difference in net capture rates was primarily the result of the increased turbidity associated with the densely packed branches delivering an increased supply of material to the polyps not facing directly into the current. Under low flow conditions, all polyps were capable of maintaining active tentacle extension, whereas under the higher flow conditions, only the sheltered downstream polyps were able to do this. For L. pertusa, the development of such high turbidity regions may be crucial for the progression of reefs from small isolated thickets to the spatially extensive reef complexes found on the Norwegian Margin, such as the Sula (Freiwald et al., 2002), Røst and Træna (Fosså et al., 2005) reefs. Flume A contained ~ 10% more polyps than flumes B and C. Polyp cup diameters within this flume tended to be slightly greater, and overall feeding area was larger. Despite this, the standard deviation in net capture rates observed across flumes for each experimental run was generally quite low. A possible explanation for this could be that the polyps in flume A, despite being more numerous and of greater diameter, were also older. Net capture rates in other cnidarians have been found to greatly reduce as maximum organism growth size is approached (Medridium senile anemones, (Anthony, 1997)). Whether this is the case with scleractinians and Lophelia pertusa in particular has yet to be investigated. Acknowledgements This work was funded by StatoilHydro and the FP6 EU-project HERMES (EC contract no GOCE-CT-2005-511234) and is a CORAMM group collaboration. The Institute of Marine Research (IMR), Norway, is thanked for allowing the sampling of coral polyps from the Tisler Reef used in this study. T. Lundälv is gratefully acknowledged for piloting the ROV during the sampling stage of this work. We also thank L. Jonsson for assistance during sampling, A. Moje, H. Wagner and G. Mirelis for lab support. This is publication 4834 of the Netherlands Institute of Ecology (NIOO-KNAW), Yerseke. [ST] References Anthony, K.R.N., 1997. Prey capture by sea anemone Metridium senile (L.): effects of body size, flow regime, and upstream neighbors. Biol. Bull. 192, 73–86. Berntsson, K.M., Jonsson, P.R., Larsson, A.I., Holdt, S., 2004. Rejection of unsuitable substrata as a potential driver of aggregated settlement in the barnacle Balanus improvisus. Mar. Ecol. Prog. Ser. 275, 199–210.

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