Optimizing heterotrophic feeding rates of three commercially important scleractinian corals

Accepted Manuscript Optimizing heterotrophic feeding rates of three commercially important scleractinian corals

Alejandro Tagliafico, Salomé Rangel, Brendan Kelaher, Leslie Christidis PII: DOI: Reference:

S0044-8486(17)31700-3 doi:10.1016/j.aquaculture.2017.10.013 AQUA 632867

To appear in:

aquaculture

Received date: Revised date: Accepted date:

23 August 2017 11 October 2017 12 October 2017

Please cite this article as: Alejandro Tagliafico, Salomé Rangel, Brendan Kelaher, Leslie Christidis , Optimizing heterotrophic feeding rates of three commercially important scleractinian corals. The address for the corresponding author was captured as affiliation for all authors. Please check if appropriate. Aqua(2017), doi:10.1016/ j.aquaculture.2017.10.013

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ACCEPTED MANUSCRIPT Optimizing heterotrophic feeding rates of three commercially important scleractinian corals.

Alejandro Tagliafico*, Salomé Rangel, Brendan Kelaher, Leslie Christidis

National Marine Science Centre, Southern Cross University, Coffs Harbour, NSW 2450, Australia.

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*Corresponding author: National Marine Science Centre, Southern Cross University, Coffs Harbour, NSW 2450, Australia.

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E-mail address: [email protected]

ABSTRACT

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Heterotrophy plays an important role in improving coral growth rate in aquaculture. While a lack of

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sufficient food will reduce growth and delay production timelines, excessive food deteriorates water quality and represents an additional production cost without benefit. Currently, there is limited

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information related to the maximum feeding rates of corals. Using the curvilinear Michaelis-Menten

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model with six different concentrations of Artemia during day and night feeding, we estimated the maximum feeding rates for Acropora millepora (4.6 ind cm-2 h-1), Hydnophora rigida (20.4 ind cm2

h-1) and Duncanopsammia axifuga (22.8 ind polyp-1 h-1) and the necessary concentrations of food

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to reach the maximum levels of feeding. Overall, the three species increased their feeding rates with

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increasing Artemia densities until the concentration reached 120 ind ml-1, after which there was no change to feeding rate. No significant differences were detected between day and night feeding rates in any of the three corals species. We demonstrate that the concentration to reach the maximum Artemia feeding rates for these commercially important coral species was above 50 ind ml-1.

Keywords: Acropora millepora; Hydnophora rigida; Duncanopsammia axifuga; feeding rate; aquarium trade; coral aquaculture

ACCEPTED MANUSCRIPT 1.

Introduction

Aquaculture provides corals for reef restoration projects, the aquarium trade, drug discovery and research (Delbeek, 2001; Leal et al. 2016), as well as contributing to employment in coastal tropical developing countries (Ferse et al., 2012; Rinkevich, 2015; Todinanahary et al., 2017). There are at least 117 coral species that have been cultivated, out of more than 300 described species (Veron et

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al., 2000; Rinkevich, 2014). However, there is limited available information related to coral feeding which is hampering efforts aimed at improving coral production (Hii et al., 2009; Wijgerde et al.,

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2011).

Heterotrophy has an important role in the energy budget of scleractinian corals because many

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nutrients that cannot be supplied by photosynthesis are acquired through feeding (Houlbrèque and

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Ferrier-Pagès, 2009). As feeding also has a positive effect on tissue and skeletal coral growth (Ferrier-Pagès et al., 2003), one of the largest challenges in intensive coral aquaculture is to find the

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optimal nutrition to achieve the fastest growth rate (van Os et al., 2012). However, there are only a

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limited number studies that have investigated coral feeding rates from an aquaculture perspective (Wijgerde et al., 2011, van Os et al., 2012), with most focusing on coral feeding in an ecological context (Anthony 1999; Houlbrèque et al., 2003; Treignier et al., 2008). Since corals often have

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species-specific conditions for optimal growth (Forsman et al., 2012), many coral species remain

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unexamined, and innovative combinations of different culture parameters require further experimental evaluation (Arvedlund et al., 2003).

Quantitative determination of food demand from cultivated corals (Lin et al., 2002) and the best time to feed them (i.e. some corals feed at night and other during the day, (Porter 1974; Borneman 2001) is desirable for cost-effective aquaculture. Long coral rearing periods makes it necessary to identify feeding regimes, times, and frequency, as well as duration of the feeding period, that maximise growth rate and survival, while minimising the financial burden of these additional

ACCEPTED MANUSCRIPT processes (Toh et al., 2014). For that reason, it is useful to know the feeding satiation point, where corals stop feeding once they have captured a certain quantity of food (Lin et al., 2002). Food addition just below this coral feeding satiation point is recommended as a strategy to reduce food wastage and avoid water quality deterioration (Ali et al., 2010).

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Artemia is a valuable live food for aquaculture because it is palatable to a great variety of aquatic organisms (including freshwater species) and can be stored in a cyst form almost indefinitely

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(Dhont and Sorgeloos, 2002). Artemia is, therefore, the most commonly used live food in

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aquaculture (Petersen et al., 2008; Dhont and Sorgeloos, 2002). Corals are also often fed Artemia (Houlbrèque et al., 2003; Yii-Siang et al., 2009) because it enhances growth and survivorship in

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both ex situ nurseries and after being transplanted to reefs in restoration projects (Toh et al., 2014).

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However, as some coral species may have an upper-prey-size limit due to their small polyp size (Houlbrèque and Ferrier-Pagès, 2009), the acceptance of Artemia should be investigated for each

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coral species considered for cultivation.

Here, we optimised Artemia feeding rates for three commercially important coral scleractinian species: (1) Acropora millepora, a reef-building species that is one of the most studied scleractinian

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coral in the Great Barrier Reef, Australia, it has commercial relevance to the aquarium trade and

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restoration projects (Borneman and Lowrie 2001; Bongiorni et al., 2011; Ramos-Silva et al., 2014); (2) Hydnophora rigida, a species with considerable demand for the aquarium trade and also used for restorations (Bongiorni et al., 2011); and (3) Duncanopsammia axifuga, a species with increasing demand in the aquarium trade and suitable for coral aquaculture (Tagliafico et al., 2017). In order to enhance ex-situ aquaculture protocols, the main objective of this study was to provide the maximum feeding rates for these three scleractinian coral species, as well as to assess whether heterotrophic feeding rates would be greater at night than during the day.

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Material and methods

This study was carried out at the National Marine Science Centre (NMSC), Southern Cross University, Coffs Harbour, Australia (30°16'3.24"S - 153°8'16.26"E). The feeding experiments were done under natural daylight (12:00 pm) and at night (after 7:00 pm) in outdoor tanks. Seawater was pumped from the adjacent open-ocean. To avoid other sources of food influencing the

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experiment, the seawater was filtered using a sand gravel filter, a 50µm filter, a cartridge particle filter (EMAUX® model CF25), a zeolite media filter (JNS model FR-2E, Japan), an in-sump protein

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skimmer (JNS model SK-6, Japan), an activated carbon media filter (JNS model FR-2E, Japan) and

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all running via a pump (Doughboy model 72543, 1HP, 18m3/h, UK). Salinity was maintained at 36 ± 0.5 ppm. Temperature was kept stable at 26 ± 0.5°C, using a temperature controller (2100L/h,

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EVO-F5, Australia).

Eight colonies of each studied species: A. millepora, D. axifuga and H. rigida (Fig. 1), were

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collected near Cairns on the Great Barrier Reefs. Each colony was acclimatized for at least one

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month and fed twice a week with Artemia. Once acclimatized, each colony was fragmented into similar size pieces using a cordless Dremel® (model 8220, USA). Fragments were fixed to glass stoppers (Vinolok, Czech) using cyanoacrylate (super glue) (Gel control, Loctite®). All fragments

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were kept for an additional month until all injuries from the fragmentation process were healed.

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Fragments were pooled and randomly selected. Only corals that appeared to be healthy (polyp fully open, rich colour and full tissue coverage) were used.

One day before commencing the feeding trials, 10 g of Artemia salina cysts (‘AAA” grade GSL Artemia Cyst, INVE, Belgium) were incubated in a 10 L well-aerated hatching cone with direct light and water at ~28°C and salinity at ~36.5 ppm. To avoid any unhatched cysts getting into the culture, a magnetised cyst collector tube was used (Sep-Art TM, INVE, Belgium). The nauplii were maintained at a density of 400 individuals/ml (ind/ml) in 8 L of filtered seawater; afterwards, the

ACCEPTED MANUSCRIPT water volume was reduced to increase the concentration of the Artemia stock (~2000 ind ml-1). Then, different aliquots of the concentrated stock and appropriate amounts of seawater were added to the vials to obtain the desired concentrations (i.e. 2, 5, 20, 50, 120 and 250 ind ml-1).

Three hours before commencing the feeding, five coral replicates for each Artemia concentration

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were transferred into independent replicate vials of 250 ml. Corals in each vial were randomly located in a recirculating water bath attached to the main tank to avoid temperature changes. Water

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movement in each vial was generated by using independent air hoses connected to glass pipets

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reaching the bottom of the vials. Water overflow was avoided during the feeding hour.

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The different volumes of concentrated Artemia were pipetted into the vials. Each coral was

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incubated with the respective Artemia concentration for one hour. After this time, five replicates of 1 ml were taken from each vial with an automatic pipet and placed in separate Eppendorf vials with

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0.5 ml of 100% Ethanol. All samples (n = 150 per species × per day time) were counted using a

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stereoscopic microscope during the following week. Feeding rates were calculated using a modification of the formula proposed by Hii et al. (2009).

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𝐹𝑒𝑒𝑑𝑖𝑛𝑔 𝑟𝑎𝑡𝑒 = (𝐼𝑛𝑖𝑡𝑖𝑎𝑙 − 𝐹𝑖𝑛𝑎𝑙 𝐴𝑟𝑡𝑒𝑚𝑖𝑎 𝑐𝑜𝑛𝑐𝑒𝑛𝑡𝑟𝑎𝑡𝑖𝑜𝑛) ⁄ 𝑆𝑢𝑟𝑓𝑎𝑐𝑒 𝑎𝑟𝑒𝑎 𝑜𝑟 # 𝑜𝑓 𝑝𝑜𝑙𝑦𝑝𝑠 × 𝑇𝑖𝑚𝑒

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The choice of normalization methods for each coral species was based on polyp size. A. millepora and H. rigida are small polyp species suited for the surface area method, whereas D. axifuga have large polyps easier to normalize with the number of polyps.

Using the Enzyme Kinetics (Michaelis-Menten model) application of SigmaPlot 13 (Systat software, San Jose, CA), the maximum feeding rates (Vmax) and Artemia densities at which halfsaturation occurs (KM) were calculated based on the feeding rates of corals exposed to six different Artemia concentrations.

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Two-way permutational analysis of variance was used to test the effects of the factors: time of day (2 levels – night and day); and Artemia concentration (6 levels – 2, 5, 20, 50, 120 and 250 ind ml-1) on the univariate response variable (feeding rate). All analyses were conducted in PRIMER (Anderson et al., 2008) using Euclidean distance similarity matrices and 9999 permutations. When

Results

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3.

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significant differences were found, appropriate post-hoc pair-wise tests were undertaken.

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Based on the curvilinear Michaelis-Menten model, maximum feeding rates (Vmax) and half– saturation constant (KM) at which corals reach those velocities were calculated for A. millepora, H.

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rigida and D. axifuga (Table 1, Fig 2). D. axifuga showed the highest feeding rates, whereas A.

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millepora presented the lowest.

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Table 1. Summary of the curvilinear regression Michaelis-Menten model of the three coral species.

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Vmax = maximum feeding rate, Km = half-saturation constant. I.C = interval of confidence.

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Hydnophora rigida

Time day night day night day night

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Species Acropora millepora

Duncanopsammia axifuga

Vmax 2.80 4.57 20.84 19.35 20.25 22.81

I.C 1.79 1.00 9.25 8.33 9.14 15.6

3.80 8.14 32.40 30.40 31.40 30.00

Km 50.58 189.20 85.80 77.01 96.22 94.70

I.C -3.07 104.23 -86.05 464.36 -31.71 203.31 -35.20 189.22 -23.34 215.79 26.87 162.54

R2 0.71 0.80 0.67 0.63 0.74 0.95

D. axifuga and H. rigida showed relatively similar Artemia concentrations to reach half of the feeding saturation or KM values. Confidence intervals for KM estimations were wide for all species, but relatively narrow for Vmax estimations; however, non-linear regressions for all species during both day and night were significant and with an R > 0.79.

R 0.85 0.90 0.82 0.79 0.86 0.90

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For each of the three coral species, feeding rates constantly increased with higher Artemia concentrations up to 120 art ml-1. After this concentration, the coral feeding rates reached saturation and stopped increasing, or even decreased in the case of H.rigida. The overall feeding rates did not differ significantly between day and night and there were no significant interactions between time

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of day and Artemia concentration (Table 2).

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Table 2. Summary of permutational analysis of variance results for three coral species fed with six

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different Artemia (Art.) concentrations during daytime and night time (Day/Night).

Pseudo-F 19.08

Hydnophora rigida

12.785

P(perm)

34.634

Day/Night

Pseudo-F P(perm)

Art. vs. Day/Night Pseudo-F P(perm)

0.0001

3.6566

0.0628

0.7884

0.5754

0.0001

2.5338

0.1183

0.8625

0.5203

0.0001

0.6369

0.4275

0.3758

0.8644

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Duncanopsammia axifuga

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Acropora millepora

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Art. concentration

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Significant differences were detected throughout growing Artemia densities. For H. rigida, all concentrations were significantly different when compared among each other and a significant reduction in the feeding rate was observed after 120 ind ml-1. Whereas for A. millepora and D. axifuga, significant differences were detected across all the concentrations, except between 120 and 250 ind/ml, indicating that a feeding saturation point was reached (Table 2, Fig. 3).

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Discussion

ACCEPTED MANUSCRIPT Coral feeding rate is dependent on prey concentration (Ferrier-Pagès et al., 2010) and, as a consequence, it increases with prey availability until a maximum feeding rate is reached (Palardy et al., 2006). When corals are fed with higher concentrations than the half-saturation constant (KM), no further increase in the feeding rate is expected (Hii et al., 2009). Consequently, feeding above this rate results in Artemia not be eaten by corals, which not only reduces cost effectiveness, but also

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causes nitrogen and phosphorous to increase in the water column, negatively affecting growth and survival (Petersen et al., 2008; Ali et al., 2010). A deterioration of water quality is particularly

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problematic for closed recirculation systems, compared to flow through systems where seawater is

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constantly refreshed (Sheridan et al., 2013). To avoid such issues in aquaculture, and to maximize

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coral growth, this study found maximum feeding rates for three commercially important species.

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For each of the three coral species investigated, feeding rate increased with food concentrations, until a maximum feeding rate was observed, beyond which ingestion stayed constant (i.e. A. millepora and D. axifuga), followed by declining feeding rates beyond the saturated point (i.e. H.

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rigida). Such results were observed after 120 ind ml-1 for all three coral species. Previous work with A. millepora on Artemia cysts did not find a saturation point for this species using a maximum concentration of 30 mg l-1 (Anthony, 1999). Another study using Artemia nauplii feed to A.

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millepora found a feeding rate of 0.13 ind polyp h-1, using a low food concentration (0.3 ind ml-1)

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and long feeding times (12 h) (Kuaniu et al. 2016). Other coral species, such as Galaxea fascicularis, have maximum feeding rates that exceed the three species in the present study (Hii et al., 2009), whereas similar results to ours have been reported for Turbinaria reniformes and Stylophora pistillata with 20 and 27 ind polyp h-1 , respectively, although using 30 Artemia per polyp as food concentration (Ferrier-Pàges et al., 2010). For the three coral species we investigated, there are no other studies providing Artemia maximum feeding rate using six different concentration of food.

ACCEPTED MANUSCRIPT Although all species of corals investigated here showed the same general patterns of feeding rate, there were species specific differences in rates of heterotrophic feeding, probably due to differences in polyp size among species, as well as variations in feeding strategies. The three coral species investigated fitted into two broad feeding strategies, as described by Lewis and Price (1975), with the small polyp species (such as A. millepora and H. rigida) feeding by combining tentacle capture

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and mucus entanglement, whereas the large polyp species D. axifuga was observed only feeding by tentacle capture. Given this, the variation in feeding rates among coral species maybe due to feeding

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mechanisms, morphology, number of tentacles and polyps, and coelenteron sizes (Johnson and

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Sebens, 1993; Hii et al., 2009). Nevertheless, it has been suggested that coral feeding effort and not necessarily polyp size or coral morphology, is a major factor in influencing species specific feeding

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rates (Palardy et al., 2005).

As water movement influences coral prey capture (Sebens et al. 1997; Forsman et al. 2012), current

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must be considered when interpreting results of coral feeding. In this study, we used an air hose

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connected to glass pipet that reached the bottom of the vials to generate water movement. This technique was an effective way to allow water and Artemia circulation throughout the vial, while maximizing the space and water volume available. Given the tight spatial constraints, this method

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was preferred to a bulk air-stone bubble diffuser makers frequently used in aquaculture systems.

The KM parameter in a coral feeding context is a direct reflection of the affinity or voracity of the coral towards certain prey, with species showing low KM values being much more voracious and capable of reaching the maximum feeding rate at lower concentrations of food, than those coral species showing higher KM values (Voet and Voet, 2011). This requires consideration for costeffective culturing of particular corals, as species that are strongly heterotrophic will growth faster and might produce up to eight times higher tissue growth and 30% higher calcification rates that those with lower feeding voracity or unfed (Ferrier-Pagès et al., 2003). However, the variation in

ACCEPTED MANUSCRIPT KM among the three species suggests that some caution is required when selecting the appropriate concentration of food to reach the maximum feeding rate. For A. millepora and H. rigida, the estimated KM appeared to be high in relation to the calculated maximum feeding rates (Vmax) and might be explained by the observed mucus release, acting as an efficient trap to increase prey capture (Naumann et al., 2009). Nevertheless, mucus trapping could affect the accuracy of the

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calculated maximum feeding rates, as not all Artermia trapped in the mucus are consumed by the corals. Consequently, the maximum feeding rate could sometimes be overestimated for coral

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species using mucus trapping.

Wild corals tend to feed at night when polyps are fully expanded (Porter, 1974; Borneman, 2001),

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which would imply additional cost related to employing aquarists to feed coral outside of normal

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business hours. However, we found no significant differences between the day and night feeding rates of the three coral species and similar results have been previously observed for other

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cultivated coral species (Hii et al., 2009; Kuanui et al., 2016). Corals most likely feed at night in

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natural environments because zooplankton densities are highest during the night (Heidelberg et al., 2004; Nakajima et al., 2008). Nevertheless, feeding activation occurs in the presence of food chemical signals (Lehman and Porter, 1973) and corals can be ‘trained’ to feed during the day,

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changing their feeding behaviour depending on the availability of food (Borneman, 2001). Our

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results corroborate these ascertains and are an important consideration for aquaculture, as night feeding may be associated with additional production costs.

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Conclusions

We estimated the maximum feeding rates of three commercially important species of coral, as well as the Artemia concentrations at which half saturation point is reached. Our results showed that corals display similar feeding rates during the day and night. This information can be used to enhance coral aquaculture protocols to obtain optimum growth rates while avoiding water quality

ACCEPTED MANUSCRIPT issues associated with overfeeding, as well as reduce additional costs associated with nocturnal feeding of corals.

Acknowledgments The authors thank D. Eggeling, A. King, C. Holloway and S. Soule for technical support. AT was

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supported through an Australian Government Research Training Program Scholarship.

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References

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Ali, M., Hayward, R.S., Bajer, P.G., Whitledge, G.W., 2010. Maintenance/Submaximum Feeding

World Aquacult. Soc. 41, 319–331.

NU

Schedules for Reducing Solid Wastes and Improving Feed Conversion in Aquaculture. J.

statistical methods. Plymouth.

MA

Anderson, M., Gorley, R., Clarke, K., 2008. PERMANOVA+ for PRIMER: guide to software and

Anthony, K.R.N., 1999. Coral suspension feeding on fine particulate matter. J. Exp. Mar. Biol.

PT E

D

Ecol. 232, 85–106.

Arvedlund, M., Craggs, J., Pecorelli, J., 2003. Coral culture - possible future, trends and directions, in: Cato, J., Brown, C. (Eds.), Marine Ornamental Species: collection, culture &

CE

conservation. Iowa State Press, Iowa, pp. 233–250.

AC

Bongiorni, L., Giovanelli, D., Rinkevich, B., Pusceddu, A., Chou, L.M., Danovaro, R., 2011. First step in the restoration of a highly degraded coral reef (Singapore) by in situ coral intensive farming. Aquaculture. 322–323, 191–200. Borneman, E., 2001. Aquarium corals: selection, husbandry and natural history. TFH Publications Inc. NJ. Borneman, E., Lowrie, J., 2001. Advances In Captive Husbandry And Propagation: An Easily Utilized Reef Replenishment Means From The Private Sector? Bull. Mar. Sc. 69, 897–913.

ACCEPTED MANUSCRIPT Delbeek, J.C., 2001. Coral Farming: Past, Present and Future Trends. Aquarium Sci. Conserv. 3, 171–181. Dhont, J., Sorgeloos, P., 2002. Artemia: basic and applied biology. Kluwer Academic Publishers, The Netherlands. Ferrier-Pagès, C., Rottier, C., Beraud, E., Levy, O., 2010. Experimental assessment of the feeding

PT

effort of three scleractinian coral species during a thermal stress: Effect on the rates of photosynthesis. J. Exp. Mar. Biol. Ecol. 390, 118–124.

RI

Ferrier-Pagès, C., Witting, J., Tambutté, E., Sebens, K.P., 2003. Effect of natural zooplankton

SC

feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs. 22, 229–240.

NU

Ferse, S.C.A., Knittweis, L., Krause, G., Maddusila, A., Glaser, M., 2012. Livelihoods of

MA

Ornamental Coral Fishermen in South Sulawesi/Indonesia: Implications for Management. Coast. Manage. 40, 525–555.

Forsman, Z.H., Kimokeo, B.K., Bird, C.E., Hunter, C.L., Toonen, R.J., 2012. Coral farming: effects

PT E

D

of light, water motion and artificial foods. J. Mar. Biol. Assoc. UK. 92, 721–729. Heidelberg, K.B., Sebens, K.P., Purcell, J.E., 2004. Composition and sources of near reef

23, 263–276.

CE

zooplankton on a Jamaican forereef along with implications for coral feeding. Coral Reefs.

AC

Hii, Y.-S., Soo, C., Liew, H., 2009. Feeding of scleractinian coral, Galaxea fascicularis, on Artemia salina nauplii in captivity. Aquac. Int. 17, 363–376. Houlbrèque, F., Ferrier-Pagès, C., 2009. Heterotrophy in Tropical Scleractinian Corals. Biol. Rev. 84, 1-17. Houlbrèque, F., Tambutté, E., Ferrier-Pagès, C., 2003. Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata. J. Exp. Mar. Biol. Ecol. 296, 145–166.

ACCEPTED MANUSCRIPT Johnson, A.S., Sebens, K.P., 1993. Consequences of a flattened morphology: effects of flow on feeding rates of the scleractinian coral Meandrina meandrites Mar. Ecol. Prog. Ser. 99, 99– 114. Kuanui, P., Chavanich, S., Viyakarn, V., Park, H.S., Omori, M., 2016. Feeding behaviours of three tropical scleractinian corals in captivity. Trop. Zool. 29, 1–9.

knowledge to ex situ production. Rev. Aquac. 8, 136–153.

PT

Leal, M., Ferrier-Pagès, C., Petersen, D., Osinga, R., 2016. Coral aquaculture: applying scientific

SC

Montastrea cavernosa. Biol. Bull. 145, 140–149.

RI

Lehman, J., Porter, J., 1973. Chemical activation of feeding in the Caribbean Reef-building coral

Lewis, J.B., Price, W.S., 1975. Feeding mechanisms and feeding strategies of Atlantic reef corals. J.

NU

Zool. 176, 527–544.

MA

Lin, M., Liao, C., Dai, C., 2002. Modeling the effects of satiation on the feeding rate of a colonial suspension feeder, Acanthogorgia vegae, in a circulating system under lab conditions. Zool.

D

Stud. 41, 355–365.

PT E

Nakajima, R., Yoshida, T., Othman, B., Toda, T., 2008. Diel variation in abundance, biomass and size composition of zooplankton community over a coral-reef in Redang Island, Malaysia. Plank. Benth. Res. 3, 216–226.

CE

Naumann, M.S., Richter, C., el-Zibdah, M., Wild, C., 2009. Coral mucus as an efficient trap for

AC

picoplanktonic cyanobacteria: implications for pelagic–benthic coupling in the reef ecosystem. Mar. Ecol. Prog. Ser. 385, 65–76. Palardy, J., Grottoli, A., Matthews, K., 2005. Effects of upwelling, depth, morphology and polyp size on feeding in three species of Panamanian corals. Mar. Ecol. Prog. Ser. 300, 79–89. Palardy, J.E., Grottoli, A.G., Matthews, K.A., 2006. Effect of naturally changing zooplankton concentrations on feeding rates of two coral species in the Eastern Pacific. J. Exp. Mar. Biol. Ecol. 331, 99–107.

ACCEPTED MANUSCRIPT Petersen, D., Wietheger, A., Laterveer, M., 2008. Influence of different food sources on the initial development of sexual recruits of reefbuilding corals in aquaculture. Aquaculture. 277, 174– 178. Porter, J., 1974. Zooplancton feeding by the Caribbean reef-building coral. Proc. 2nd. Int. Coral Reef Symposium. 2, 111–125.

PT

Ramos-Silva, P., Kaandorp, J., Herbst, F., Plasseraud, L., Alcaraz, G., Stern, C., Corneillat, M., Guichard, N., Durlet, C., Luquet, G., Marin, F., 2014. The Skeleton of the Staghorn Coral

RI

Acropora millepora: Molecular and Structural Characterization. PLOS ONE. 9, e97454.

SC

Rinkevich, B., 2014. Rebuilding coral reefs: does active reef restoration lead to sustainable reefs? Curr. Opin. Environ. Sustain. 7, 28–36.

NU

Rinkevich, B., 2015. Novel tradable instruments in the conservation of coral reefs, based on the

MA

coral gardening concept for reef restoration. J. Environ. Manage. 162, 199–205. Sebens K.P., Witting, J., Helmuth, B. 1997. Effects of water flow and branch spacing on particle

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Biol. Ecol. 211, 1–28.

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capture by the reef coral Madracis mirabilis (Duchassaing and Michelotti). J. Exp. Mar.

Sheridan, C., Kramarsky-Winter, E., Sweet, M., Kushmaro, A., Costa, M., 2013. Diseases in coral aquaculture: causes, implications and preventions. Aquaculture. 396-399, 124–135.

CE

Tagliafico, A., Rangel, S., Kelaher, B., Scheffers, S., Christidis, L., 2017. A new technique to

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increase polyp production in stony coral aquaculture using waste fragments without polyps. Aquaculture in press https://doi.org/10.1016/j.aquaculture.2017.09.021 Todinanahary, G.G.B., Lavitra, T., Andrifanilo, H.H., Puccini, N., Grosjean, P., Eeckhaut, I., 2017. Community-based coral aquaculture in Madagascar: A profitable economic system for a simple rearing technique? Aquaculture. 467, 225–234. Toh, T.C., Ng, C.S.L., Peh, J.W.K., Toh, K.B., Chou, L.M., 2014. Augmenting the PostTransplantation Growth and Survivorship of Juvenile Scleractinian Corals via Nutritional Enhancement. PLoS ONE. 9, 1–9.

ACCEPTED MANUSCRIPT Treignier, C., Grover, R., Ferrier-Pagès, C., 2008. Effect of light and feeding on the fatty acid and sterol composition of zooxanthellae and host tissue isolated from the scleractinian coral Turbinaria reniformis. Limnol. Oceanogr. 53, 2702–2710. van Os, N., Massé, L., Séré, M., Sara, J., Schoeman, D., Smit, A., 2012. Influence of heterotrophic feeding on the survival and tissue growth rates of Galaxea fascicularis (Octocorralia:

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Occulinidae) in aquaria. Aquaculture. 330–333, 151–161. Veron, J.E.N., 2000. Corals of the world (Vol. 1). M. Stafford-Smith (Ed.). Australian Institute of

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Marine Science. Townsville.

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Voet, D., Voet, J., 2011. Bioquemestry, 4th Edition. Wiley, NJ.

Wijgerde, T., Diantari, R., Lewaru, M., Verreth, J., Osinga, R., 2011. Extracoelenteric zooplankton

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feeding is a key mechanism of nutrient acquisition for the scleractinian coral Galaxea

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fascicularis. J. Exp. Biol. 214, 3351–3357.

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Figure 1. Coral species used in the present study, with details on polyp size. From top to bottom: Acropora millepora, Hydnophora rigida and Duncanopsammia axifuga

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Figure 2. Feeding rates as a function of Artemia concentration for three coral species during the day and the night. Data shows the mean ± standard error. Black lines show the best fit to the curvilinear

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Michaelis-Menten regression model and blue lines represent 95% confidence limits

Figure 3. Comparisons of feeding rates of three different coral species under different

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concentrations of Artemia, as well as comparisons of feeding rates during the day and the night.

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Bars represent the means (± SE) of the main effects, as there were no significant interaction between day/night time and Artemia concentrations. Significant groups (at P < 0.05), derived from

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The optimal feeding rates of Artemia to three different species of commercial scleractinian corals (Acropora millepora, Hydnophora rigida and Duncanopsammia axifuga) was determined.

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Time of day (midday or night) had no significant effect on the feeding rates for Acropora

Maximum Artemia feeding rates (Vmax) for three different species of commercial

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scleractinian corals were calculated.

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millepora, Hydnophora rigida and Duncanopsammia axifuga.