Effects of sediment on the energy budgets of four scleractinian (Bourne 1900) and five alcyonacean (Lamouroux 1816) corals

Journal

ELSEVIER

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY

of Experimental Marine Biology and Ecology 186 (1995) 259-275

Effects of sediment on the energy budgets of four scleractinian (Bourne 1900) and five alcyonacean (L amouroux 18 16) corals Bernhard

Riegl a,b3*, George

M. Branch a

“Coastul Ecology Unit, Zoology Department. University of Cape Town, Rondebosch, 7700 South Africa “OceanographicResearch Institute. P.O. Box 10712, Marine Parade, Durban, South Africa Received

24 November

1993; revision

received 4 October

1994; accepted

13 October

1994

Abstract

The physiological reactions to sediment of four scleractinia and five alcyonacea from South Africa were observed in the laboratory. Species tested were Fuviufavus Forskal, Favitespentagona Esper, Platygyra daedalea Ellis & Solander, Gyrosmilia interrupta Ehrenberg, Lobophytum depressum Tixier-Durivault, Lobophytum venustum Tixier-Durivault, Sinularia dura (Pratt), Sinularz’u leptoclados (Ehrenberg) and Sarcophyton gluucum (Quoy & Gaimard). Natural sedimentation levels and light conditions were simulated. Photosynthetic carbon production and respiration were measured by respirometry. Loss of fixed carbon through mucus production was measured directly by filtration. The results were used to mode1 daily energy budgets for these species. One set of models allowed for 50% PARS (photosynthetically active radiation at the surface), another set of models allowed for 25 y0 PARS. The models showed severely diminished productivity and decreased respiration under sedimented conditions. Production/respiration (P/R) ratios of all species were above 1 in the absence of sediment and dropped below unity when the corals were subjected to sedimentation. Although overall respiration dropped, its demand upon the also diminished amount of photosynthetically produced carbon rose dramatically. Without sediment, mucus output averaged 35% of daily respiration; this rose to 65% when sediment was applied. Sediment affects coral metabolism by decreasing photosynthetic production, increasing relative respiration and increasing carbon-loss through greater mucus output. Keywords: Effects of sediment; Coral; Stress; Mode1

* Corresponding

author.

Present

Physiology;

address:

Energy budget;

Florianigasse

50/l/2,

Mucus;

Scleractinia;

1080 Wien, Austria.

0022-0981/95/$9.50 0 1995 Elsevier Science B.V. All rights reserved SSDI 0022-0981(94)00164-2

Alcyonacea;

260

B. Riegl, G.M. Branch /J. Exp. Mar. Bid. Ecol. 186 (1995) 259-275

1. Introduction Numerous studies have described the behavioural and growth reactions of scleractinia to sedimentation (Bak & Elgershuizen, 1976; Lasker, 1980; Rogers, 1983; Laboute, 1988; Rice & Hunter, 1992; Stafford-Smith & Ormond, 1992; Stafford-Smith, 1993), but relatively few studies exist on their physiological responses. The literature indicates that sediment severely interfers with coral energetics (Szmant-Froehlich et al., 198 1; Dallmeyer et al., 1982; Abdel-Salam & Porter, 1988), but further information about the mechanisms of interference is needed. Sediments could reduce available light and, therefore, photosynthetic production, and sediments could increase respiration because of increased activity of the polyps (Bak & Elgershuizen, 1976; Stafford-Smith, 1993) or due to increased mucus output. The importance of mucus for coral energetics has long been recognized (Benson & Muscatine, 1974; Richman et al., 1975) and anecdotic observations on increased mucus production due to sedimentation are plentiful (Bak & Elgershuizen, 1976; Rogers, 1990; Stafford-Smith & Ormond, 1992; Stafford-Smith, 1993). However, a quantification of possible changes in mucus output has not yet been attempted. The present study attempts to quantify the importance of each of several responses to sediment. Using a modelling approach the coral’s reactions are integrated to provide estimates of the influence of sediment on daily energy budgets. Most physiological studies of sediment response have been performed on Atlantic hard coral species (Szmant-Froehlich et al., 1981; Dallmeyer et al., 1982; Peters & Pilson, 1985; Abdel-Salam & Porter, 1988) while little information is so far available on Indo-Pacific species (Yamasu & Mizofushi, 1989). Equivalent studies with soft corals have not been made. The literature includes only speculation and indirect evidence concerning the tolerance of soft corals to sediments (Schuhmacher, 1975; Dinesen, 1983; Dai, 1991; van Katwijk et al., 1993). The aims of this study were: (1) to assess differences in productivity and respiration under sedimented and unsedimented conditions in selected hard and soft coral species; (2) to model the effects of sedimentation under light conditions corresponding to different depths or to different degrees of light penetration; (3) to test for differences in mucus production under sedimented and unsedimented conditions; (4) to quantify carbon loss due to mucus production; (5) to identify which component of the effects of sedimentation creates stress, and (6) to see whether differences exist in the physiological reactions of the tested species.

2. Methods We used corals collected from 4- and 9-Mile Reefs in the Maputaland reef systems in northern Natal, South Africa (Fig. 1). Nine species were studied: four scleractinia Favia favus, Favites pentagona (plocoid calyx arrangement), Platygyra daedalea, Gyrosmilia interrupta (meandroid calyx arrangement) and five alcyonacea Lobopthytum pat&m, Lobophytum depressum, Sir&aria dura, Sinularia leptoclados and Sarcophyton glaucum. These species were chosen for their differences in growth form and for their

B. Riegl, G.M. Branch /J. Exp. Mar. Biol. Ecol. 186 (1995) 259-275

28”OO’ -

261

v

28”00’-

Fig. 1. The reef system off the Maputaland coast in northern Natal, South Africa. Corals grow on fossilized dunes parallel to the coast. Experimental corals were collected in the Central Reef Complex.

differences in their typical habitats on the reefs (Riegl et al., 1995). All scleractinia were commonly found in areas of high sedimentation where alcyonacea were generally rare. In alcyonacea, different growth forms were represented: leathery growth with a completely flat surface (L. depressum), with ridges (L. pat&m, Sinularia duru), with fingerlike projections (Sinuluriu leptocludos); an erect mushroom shaped growth form (Sarcophyton glaucum). Six colonies of each species were collected and brought back to the laboratory in Durban. The corals were maintained in flow-through, open circuit tanks containing filtered sea water at a constant, thermostat-regulated temperature of 21 “C. Light levels in the experimental aquaria were similar to those measured on the reefs. This was achieved by placing the holding tanks under corrugated plastic roofing and shade-cloth until light intensities in the tanks matched those on the reefs. Light intensities were measured with a LI-COR Model 185 quantum photometer/radiometer, fitted alternatingly with an underwater and above-water PAR-probe. Corals were allowed to adapt to laboratory conditions for 6 wk prior to the experiments.

B. Riegl. G.M. Branch 1 J. Exp. Mar. Bid. Ed.

262

2.1. A4easurements

ofproductivity

186 (1995) 259-275

and respiration

Oxygen production and respiration were measured using a 7-chambered respirometer. Each chamber was fitted with a stirring pedal, driven by an electrical motor, and a YSA model 57 Oxygen probe allowing simultaneous readings of dissolved oxygen levels in all 7 chambers. In order to assure accuracy, the oxygen probes were standardized using Winkler-titrations (Strickland & Parson, 1972) prior to each test series. The chambers were maintained at a constant temperature of 21 “C, comparable to the average winter water temperature of the Agulhas current, within which the reefs are situated (Schumann, 1988; Beckley & van Ballegooyen, 1992). All corals were collected and the experiment was conducted in mid-winter (July/August). Productivity and respiration were measured on the same corals under identical light regimes with and without sediment. Replicate data were obtained from 4 to 6 corals in each species in 5 runs for each light intensity with and without sediment. In production experiments, the baseline from which O,-increase was measured was set at ambient oxygen saturation, which was between 80 and 85 “/ (6.1 ppm). In respiration experiments corals were allowed to respire until oxygen levels had dropped to 50”/, saturation, as previous tests had shown that over this range the falling oxygen concentration had no effect on the respiration rate. Similar findings are also reported in the literature (Spencer-Davies, 1991). Each experimental run was 20 min long and repeated 5 times. Photosynthesis was measured under five different light levels. Light levels were measured using a LI-COR 185 quantum radiometer/photometer connected to an underwater probe and an above-water probe (LI 190, LI 192). The low light levels (46 and 184~mol~m~*.s~‘) were provided by a bank of four full spectrum daylight tubes (Astra 4OW, B 2.1 Colour match/55), mounted over the respirometer chambers, which were enclosed by white, reflecting surfaces to allow homogenous reflection. The other light intensities (345, 690, 1380 pmol. mm2. s -’ were obtained by differential shading in daylight, using shade cloth (Titlyanov, 1991). Immediately after each oxygen production measurement, the respirometry chambers were covered in black plastic and respiration was measured. Thus the measurements of the respiration rate could be related to a previously measured photosynthetic rate. At the end of the experiments all corals were fixed in formaline-saline for 24 h, then transferred to 70”! alcohol and later decalcified in a solution of 15 “4 sodium citrate and 50% formic acid in order to obtain the tissue weights. Decalcification took between 12 and 24 h. Wet tissue weight was determined by weighing the decalcified corals after they were squeezed dry and repeatedly placed for one minute on a water absorbing cloth in order to remove all excess water. Tissues were weighed only when no more water could be extruded from them. 2.2.

Sediments

Sand collected on the same reefs as the corals was burnt in a muffle furnace at 350 “C for 2 h to eliminate the organic component. A grain size analysis using a settling tube showed it to consist of 0.1% very coarse sand (grain size > 1000 pm), 0.69; coarse

B. Riegl. G.M. Branch /J. Exp. Mar. Bid. Ed.

186 (1995) 259-275

263

sand (500-1000 pm), 46.1 y0 medium sand (250-500 pm) and 53.4% fine sand (125250 pm); medium grain size was 253 pm. Of the clean sand, a constant quantity of 14.18 g, which amounted to a sediment load of 200 mg . cmm2 for the respiration chamber (bottom area= 70.9 cm2, therefore: 70.9 x 200 mg = 14.18 g), was applied to the corals. This sedimentation level was chosen because it compared well to the observed sedimentation levels on South African reefs (Riegl, 1995) and also because it had been used in previous and parallel studies (Rogers, 1990; Stafford-Smith, 1993; Riegl, in press.). The sediment was spread as evenly as possible over the bottom of the jars and the corals, which were of different sizes and shapes, covering them with comparable amounts of sand. This ensured that a constant quantity of sand was confined within the respiration chamber and that the corals were covered with a comparable layer of sand. 2.3. Mucus analysis Before each respirometry incubation began, the colony surface was cleaned of organic and inorganic materials with a gentle stream of filtered sea water. The specimens were placed at ambient temperature in sterilized containers with 500 ml 0.2 pm filtered sea water for 3 h. Oxygen saturation of the water was 83%, determined by Winklertitrations (Strickland & Parson, 1972) and lighting was constant at around 230 ~mol*m~2.s-‘. For control conditions, each coral was placed in a jar and left for 3 h. Then corals were removed from the jars and the water was stirred for 5 minutes to aid mucus precipitation (Herndl & Velimirov, 1985). The water was filtered through a preweighed filter (47 mm diameter, 0.2 pm pore size), rinsed first with ammonium formate (to elute salt residues and stop bacterial activity) then with 0.5 N H,SO, (to elute free carbon) and finally with 5 ml distilled water. The filters were dried in a drying oven at 70 “C for 24 h and then weighed. For conditions with sediment application the corals were placed in a preweighed, premuffled aluminium dish in sterilized jars, and 14.18 g sterile sediment was applied (equivalent to 200 mg * cm-2). After 3 h all sediment was collected off the corals which were removed. The water was stirred for 5 min to aid mucus precipitation, then decanted and filtered as described above. The trays containing the sediment were dried for 24 h at 70 “C, weighed, and afterwards burned at 350 “C for 1.5 h. They were then reweighed. The weight difference before and after muffling gave an indication of the weight of mucus adhering to the sediment. Carbon content of the mucus was determined by burning filter samples with mucus in a helium/oxygen flame in a Perkin-Elmer 2400 CHN Micro Analyser. All data are based on two experimental runs with five corals per species. 2.4. Modelling We used numerical models to integrate all measurements of the coral’s responses to sedimentation. As the experiment was conducted in mid-winter, light conditions for a clear, cloudless mid-winter day (July) were used for modelling 24 h production. Sur-

264

B. Riegl, G.M. Branch /J. Exp. Mar. Bid. Ed.

186 (19951259-275

face irradiance was measured with a LI-COR 185 quantum radiometer/photometer connected to an above-water probe (LI 190) taking hourly readings over the entire daylight period starting one hour before dawn and ending one hour after dark. Irradiance readings in W. m m2 were converted by a factor of 4.6 to arrive at the PAR (photosynthetically active radiation) relevant unit pmol . rn-*. s -’ (Biggs, 1984). Measurements over 3 days were averaged to provide the light intensities for the model day. Maximum irradiance levels in Natal are around 2760 pmol . rne2. s ml in Winter and 4600 pmol . m-2. s -’ in summer. This is comparable to values reported by Titlyanov (1991) from the central Indian Ocean. The light conditions on the reefs were measured during the winter and spring months June, July, August and September at 10m depth, using the same LI-COR 185 radiometer/photometer connected to an underwater probe (LI- 192). Light attenuation at 10 m depth was found to vary between 50 and 75 %. Using these measurements, the experimental procedure and the frame for the modelling exercise employed 1380 ~mol~m~2.s-1 as maximum irradiance for production measurements. This level corresponds to maximum irradiance for winter at a 10 m-deep site (50% light attenuation), when the water is usually clear, and for summer, when the water is usually murky (75% attenuation). The other light levels used in the experiment and the numerical model were chosen to provide more or less equally interspersed data points between the extremes (46 ~mol.m~2.s-1 to 1380 ~mol~m-2.s-‘). The theoretical irradiance curves for the models were calculated from data for 25 % and 50% of surface irradiance (Fig. 2). Using these assumptions, energy budgets could be calculated for theoretical sites at 10 m (50% PARS) and 15 m depth (25% PARS) in clear water conditions, and at 10 m in murky conditions (25% PARS). For the calculation of daily production and respiration, the data from the laboratory experiments were used. The productivity and respiration data points obtained in the laboLight attenuation due to sediment cover

100 90 -0

100

mg

200 mg

mg.cm

-2

300mg

400’mg

500’mg

sediment cover

Fig. 2. Light attenuation caused by different levels of sediment an attached irradiance meter, simulating a flat coral.

application

onto a flat Plexiglas

plate with

B. Riegl, GM.

Branch /J. Exp. Mar. Bid. Ed.

186 (1995) 259-275

265

ratory under a fixed light regime were assigned to the time of the day when similar light intensities were observed. Thus a bell-shaped curve with productivity and corresponding respiration data for maximum and minimum PAR as well as two intermediate points in the morning and afternoons was obtained (PAR at time of day in pmol . m -2. s -‘: o-0500: 0,060O: 46,070O: 184,080O: 345,090O: 690, noon: 1380,160O: 690, 1700: 345, 1800: 46, 1900-2400: 0. A smoothed curve was laid through the datapoints. The same was done with respiration data corresponding to each production data point. The areas under the bell-shaped curves was calculated to provide an estimate of total production and respiration over a 24-h period. From these values daily P/R ratios were calculated. Mucus production was assumed to be constant over the full 24-h period (Crossland et al., 1980). 3. Results 3.1. Eflect of sediments on available light Light attenuation by various loads of sediment was measured by spreading the sediment across a Plexiglas plate, under which a light sensor was attached. Results showed that 100 mg sediment. cmm2 on a flat surface caused a 75% reduction in available light. Light reduction approached a maximum (97 %) at 400 mg.cm -’ and was not further reduced at 500 mg . cmm2 (Fig. 2). 3.2.

Overall productivity and respiration characteristics

Productivity and respiration data are given in Table 1. They were analyzed by means of factorial Analysis of Variance (Zar, 1984) to test for the influence of species, individuals, replicates (with replicates being nested into individuals), light, sedimentation and the interaction between light and sedimentation on productivity and respiration. Individuals and replicates had no influence on either productivity (P) or respiration (R) in the presence or absence of sediment, demonstrating homogeneity between individuals and replicates (scleractinia: P without sediment: F= 0.19, df3, p = 0.9, with sediment: F = 1.01, df:12, p = 0.44, R without sediment: F = 0.58, df:3, p = 0.63, with sediment: F= 1.18, df:12, p = 0.29; alcyonacea: P without sediment: F= 0.15, df:3, p=O.92, with sediment: F=0.61, df:3, p=O.86; R without sediment: F=O.84, df:3, p=O.47, with sediment F=0.67, df14, p=O.81). In scleractinia as well as alcyonacea significant influences on productivity were exerted by sediment (scleractinia: F= 18.21, dfzl, p = 0.001; alcyonacea: F= 36.8, df:l, p = O.OOl), light level (scleractinia: F= 23.51, df:4, p = 0.001; alcyonacea: F= 56.5, df4, p = 0.001) and interaction of sand with light, when both factors were modelled as equally weighed (scleractinia: F = 2.77, df:4, p = 0.027; alcyonacea: F = 2.62, df4, p = 0.034). In scleractinia these factors also significantly influenced respiration (sediment: F018.2, df:l,p = 0.0001; light: F= 23.5,df:4,p = 0.0001; sediment*light: F= 2.77, df:4, p = 0.02). In alcyonacea only the interaction of sand and light had a significant influence on respiration (F= 3.24, dfz4, p= 0.012). This situation is reflected in Table 2.

(pgC

Productivity

and respiration

5.9 1.9 1.6 I.5 8.3

- 8.4 + 8.6 4.7 If-4.3 4.6 5 6.9 -2.7i7.1 5.6 f 8.6

1.7 + 2.0 11.9+5.6 - 10.4 + 3.5 14.7 c 4.6

PC\Ki1

+ SD)

9.9 5.2 3.1 5.6 18.2

17.3 22.4 14.6 27.6

2 8.6 * 3.9 k2.4 _t 2.8 + 16.9

t_ 4.2 + 8.8 2 10.0 i 6.0

Rcsed1

I day

‘,

2.7 2.3 3. I 3.5 10.5

2 10.4 i 8.9 i 5.2 _t 8.5

_t 4.6 & I.9 + 3.7 _t 5.3 + 11.0

+ 11.2 + 9.1 & 7.7 + Il.9

3.3 * 4.3 f 6.4 k 9.1 * 14.9*

23.2 15.4 12.2 22.0

R, 2

6.9 4.5 4.3 9.6 13.2

18.9 21.6 11.5 14.4

PC2 t 15.2 _t 5.8 f 6.9 f 8.5

2

4.5 _t 3.9 4.9* 1.9 3.52 1.7 5.1 _t 1.4 16.8 f 9.6

12.1 + 10.6 15.5 f 7.9 7.124.7 15.126.7

kcd

- 1.1 + 5.4 3.6 ?r 2.8 3.1 _t 2.3 3.5 f 2.5 3.6~ 13.5

6.4 6.1 4.1 2.5

PCsrd2

13.7 6.2 7.9 1.1 9.1

26.8 20.3 23.0 24.1

_t 6.7 k 1.5 f 3.7 _t 2.0 + 2.2

+ 6.7 5 6.X _t 8.7 k 3.9

Rc 3

12.6k6.3 14.1 f 5.6 11.6i2.8 17.9-tl.7 23.9+ 5.2

44.5 _t 13.3 33.7 i 13.6 38.1+20.1 27.5 * 7.8

PC. 3

* 3.1 i 6.9 & 9.1 f 5.2

ll.O_t5.9 5.7 2 3.7 7.3 _e3.6 7.5 * I.5 9.3 & 3.2

14.1 13.0 15.5 15.6

Rc,ed 3

0 2.0 i 4.7 4.6 k 2.9 7.1 & 5.4 105~11.8

15.1+10.4 4.6? 17.4 20.4kl7.6 _

3

13.3 6.1 4.2 1.4 13.1

_t 14.1 i4.2 i 3.9 + 4.6 f 7.5

24.9 i 8.9 38.5 k 8.5 25.1+ I9 21.224.8

R, 4

18.9 _t 17.1 14.1 2 6.6 12.6 _c5.3 18.6* 12.9 25.9k11.7

42.6& 17.3 59.2i36.7 42.9k19.8 31.7~ IO.6

PC 4 4

4.7 23.3 7.8 8.3

4

8.0 k 3.9 4.4~ 1.6 5.8 i 4.9 5.7 _t 2.9 13.4 i 17.3

18.4 k 24.9 k 19.7 + 18.9i

ksed

12.7 k 9.7 Il.4+ 5.5 10.2 5 4.4 12.8i_6.7 23.1_+16.1

5

_t 14.2 f 32.5 k 8.5 i 21.6

10.8 + 6.9 1.9 & 6.7 6.0 f 3.4 5.6 2 2.3 22.Oi 14.5

40.7 47.7 34.1 28.8

Rc 5

26.0 k 6.9 19.7* 9.0 11.2 * 4.5 30.3 f 11.5 35.3239.1

67.9k20.2 64.42 14.7 69.3i26.1 66.2+ 12.9

p,

5

i i f i

10.5 22.5 11.9 7.3

5

6.9 + 1.9 5.5 * 4.9 3.5k4.1 7.8 k 2.3 26.3 + 31.0

35.8 33.0 23.7 33.8

J&i

13.6 f 13.2 14.22 11.7 9.4 + 2.8 17.7 k 9.3 48.6k55.5

41.5 i 13.3 35.8k20.0 41.9k18.3 40.75 14.8

PCsed

light level (1:46, 2: 184, 3: 345,

24.2i8.1 28.9i50.2 27.4t16.1 24.8i 17.2

PCsed

sediment for each experimental

PCsed

for all corals without (PC. R,-) and with (Pclcd, RcrrJ

given in pg. C. g,,,,,,

8.6 + 4.1 * 4.2& 3.4 + 12.2 i

18.4-t 1.0 17.3 & 8.3 10.7 i 9.6 24.1 _t 9.3

Rc 1

1 h

’

’ k SD)

6.8 4.1 2.4 10.3

0.8 _t 5.1 0.2 2 6.8 2.0 * 3.7 6.3-tl.X 10.1 k21.7

5.6 2 1.3 * 3. I i -4.9&

PC 1

gci,ral1 h

(pgC g,,,,,

L. depressum L. venu.wm Sinuluricr leptocludos Simlaria duru Sarcophytoii glaucum

Alqonacea:

Fu via fu vus Favites pentagona P. daedalea G. imerrupta

Scleructmict:

(B) Respiration

gbucwn

ciurn

Sarcophwm

Sinuluriu

L. depressum L. wnustum Sinularia leptocltrdo~

Alcwnacea:

Fu riu fu I’US Favites pentagona P. dtteduleu G. interrupta

Sclerrrctinia:

(A) Productivity

Table 1 Production and respiration characteristics 4: 690, 5: 1380 /Imol.m~‘~s~‘)

0.59

0.53

0.45

P. daedalea

G. interrupta

0.12

0.25

0.37

Sinularia dura

Sinularia leptoclados

Sarcophyton glaucum

0.41

0.35

0.26

P. daedalea

G. interrupta

0.12

0.10

0.17

0.24

L. venusturn

Sinularia dura

Sinularia leptoclados

Sarcophyton glaucum

0.05 0.05 0.06 0.07 0.14

0.17 0.14 0.20 0.13

25% PARS

0.10 0.11 0.09 0.13 0.25

-63% - 58% -40% - 55% -42%

- 56% -64% -43% - 50%

- 30% - 52% -30% -46% -32%

- 38%

-41%

0.32

0.28

-55”/,

-46%

0.21 0.12 0.15 0.15 0.23

0.49 0.47 0.40 0.50

0.21 0.13 0.13 0.14 0.29

0.59

0.46

0.58

0.55

R without ( + or - ) sediment mg.Cggt.dmt

P change

0.27

0.30

sediment mg.Cgg’.d-’

P with

50% PARS

0.19 0.12 0.12 0.14 0.25

0.37 0.41 0.35 0.41

0.18 0.11 0.12 0.14 0.29

0.48

0.36

0.45

0.46

sediment mg.Cgmt.dmt

R with

0

~8% + 7%

-9% + 2% - 16%

-23% - 13% - 13% - 18%

-1%

-4%

- 11% - 13%

- 15%

-22%

- 17% -22%

0.63 1.01 0.71 1.11 1.06

0.51

0.88

0.88

0.78

0.98 1.28 0.95 1.70 1.27

1.03 1.03 1.17 0.80

24 h P/R ( + or - ) without sediment

R change

0.25 0.41 0.50 0.54 0.57

0.31

0.56

0.35

0.48

0.53 1.05 0.73 0.90 0.87

0.65 0.59 0.87 0.58

with sediment

24 h P/R

1.38 2.33 3.00 2.57 1.92

1.47

1.72

1.55

1.45

2.60 2.71 1.83 5.35 1.85

1.67 1.36 2.02 2.27

Noon P/R without sediment

1.50 2.75 2.00 2.40 1.77

1.33

1.42

1.21

1.33

1.85 2.80 3.00 2.20 1.59

1.17 1.06 1.78 1.19

Noon P/R with sediment

The values of Table 1 were integrated over a 24-h period. 24 h PC and R, values correspond to the area under a hyperbolic curve characterized by hourly PC and Rc values at the following light levels at corresponding time of the day: PAR at time of day in pmol m - 2. s- ‘: O-500: 0, 0600: 46, 0700: 184, 0800: 345, 0900: 690, noon: 1380; 1600: 690, 1700: 345, 1800: 46, 1900-2400: 0.

0.13

L depressum

Alcyonacea:

0.38

Favites pentagona

Scleractinia:

Favia favus

and respiration,

0.16

L. venusturn

(B) 24-hr C-productivity

0.21

L. depressurn

Alcyonacea:

0.57

Favites pentagona

P without sediment mg.Cgg’.d-’

and respiration,

Faviafavus

Scleractinia:

(A) 24 hr C-productivity

Table 2 Results of the energy budget models

5

268

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186 (1995) 259-275

Species differed in respiration (scleractinia: F = 4.07, df:3, p = 0.0072; alcyonacea: F = 39,3, df:4, p = 0.0001). A subsequent Tukey test for studentised range showed that differences in respiration existed between the sclearactinia Favites pentagona and Platygyra daedalea, but not among the other scleractinian species and between the alcyonacean Sarcophyton glaucum and all other alcyonacean species, which formed a homogeneous group. Respiration in scleractinia differed significantly from that in alcyonacea (F= 73.3, df:8, p = 0.0001). In scleractinia, productivity did not differ between species (F = 2.18, df:3, p = 0.09) but in alcyonacea it did (F= 14.5, df:4, p = 0.001). A subsequent Tukey test for studentized range showed Sarcophyton glaucum to differ from all other alcyonacean species. Productivity differed significantly between alcyonacea and scleractinia (F = 27.3, df:8, p = 0.0001). The photosynthesis/irradiance relationship suggested that most species were not fully saturated at an irradiance level of 1380 pmol . m m2. s -l, only Sinularia dura appeared to saturate at 690 pmol . m -2 s ~‘. Alcyonacea had lower productivity than scleractinia (Table 2). Overall, the results can be summarized as follows. Alcyonacea were less productive than scleractinia, there were no differences in productivity among scleractinia, but differences between Sarcophyton glaucum and the other alcyonacea. In scleractinia and alcyonacea the application of sediment significantly reduced productivity as well as respiration (Table 1). 3.3. Modelling species responses to sedimentation

in dtzerent light regimes

We based our models on a cloudless Natal mid-winter day. Total carbon productivity and respiration were calculated for two scenarios: 50% irradiance loss on the community, as could be expected in very clear conditions on a shallow coral community, and 75% irradiance loss, as could be expected in murky conditions. In both cases scleractinia produced and respired significantly more than alcyonacea (t-test, t = - 4.57, p = 0.0025). All models show clearly that scleractinia produce far more carbon per unit tissue than alcyonacea (Table 2 A,B). Serious losses in photosynthetic productivity were due to coverage by sediments. These ranged in scleractinia from 38% (Gyrosmiha interrupta) to 46% (Faviafavus) with an average of 45% ( t 8% SD) for 50% PARS (Table 2A) and from 43% (Platygyra daedalea) to 64% (Favitespentagona) with an average of 53 “/, ( + 9% SD) for 25 y/, PARS (Table 2B). The differences in productivity loss between the two models were not significant (U-test, z = 1.5, p> 0.05). Productivity losses in alcyonacea ranged from 30 y0 (Lobophytum venustum, Sinularia dura) to 52% (Lobophytum depressurn) with an average of 38% (+ loo/, SD) for 50% PARS (Table 2A) and from 40% (Sarcophyton glaucum) to 63% (Lobophytum depressum) with an average of 52% (t 10% SD) for 25% PARS (Table 2B). The differences between the proportional losses for the two scenarios were not significant (U-test, z = 0.89, p = 0.07). In general, also decreases in respiration were observed with sedimentation. They ranged in scleractinia from 15 y0 (Gyrosmilia interrupta) to 22% (Platygyra daedalea,

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Favites pentagona) with an average of 19% (k 3% SD) for 50% PARS (Table 2) and from 13% (Favites pentagona and Platygyra daedalea) to 23% (Favia favus) with an average 16% ( f 5% SD) for 25% PARS (Table 2). The differences between the proportional losses for two models were not significant (U-test, z = -0.5, p = 0.61). In alcyonacea they ranged from 0 y0 (Sinularia leptoclados, Sarcophyton glaucum) to 13 y0 (Lobophytum venustum) with an average of 6% ( + 6% SD) for 50% PARS (Table 2). In 25 y0 PARS respiratory increase by 2 y0 were observed in Lobophytum venustum and by 7% in Sarcophyton glaucum. The other three species showed respiratory decreases by an average of 11% ( + 4% SD; Table 2). There were no significent differences in the percentage respiratory decreases between the two models (U-test, z = 1.7, p = 0.07). The decreases in respiration were however not as high as those in productivity (Table 2). Therefore, the proportional C-loss due to respiration increased under sedimentation. P/R ratios (Table 2 A,B) calculated for maximum irradiance at noon showed that under these conditions all species were autotrophic both with and without sediment cover in the 50% PARS as well as the 25% PARS model. In the absence of sediment cover, and with 50% PARS, P/R ratios over 24 h showed three species (Gyrosmilia interrupta, Lobophyton depressum, Sinularia dura) to be heterotrophs, although they had a P/R ratio only slightly below 1. Under sediment and with 50% PARS, all but one of the species (Lobophytum venustum) had P/R ratios well below 1. In the 25 y0 PARS model three species (Lobophytum venusturn, Sinularia leptoclados, Sarcophyton glaucum) had P/R ratios above 1 in the model without sediment. With sediment all species were below 1. 3.4.

Carbon loss due to mucus production

The results from the mucus measurements are summarized in Table 3. Overall, scleractinia, except Platygyra daedalea, produced more mucus than the two tested alcyonacea. The percentage of respired carbon allocated to mucus production was lower in the scleractinia, as their overall respiration was much higher than in the alcyonacea (Tables 2 and 3). With sediment application, mucus production increased in all corals except Platygyra daedalea and Lobophytum venustum. The differences between the percentage of C lost to mucus production in sedimented and unsedimented conditions were significant for all investigated species (U-test, z = 2.041, p = 0.041). In the absence of sediment, mucus production accounted for the lowest share of daily respiration in Platygyra daedalea (16%), the highest in Lobophytum venustum (74%). When sediment was applied, the lowest percentage was again in Platygyra daedalea (16%) the highest in Sinularia dura (91%, Table 3). Proportional carbon losses in daily productivity and respiration due to mucus production were not significantly different between the models for 50% and 25% PARS (U-test, z = 1.21, p = 0.22 for respiration and production, respectively). Carbon content of the total mucus adhering to the sediment and forming a mucous sheet was very high and accounted in most species for more than a full day’s production, ranging from only half a day’s net production in Favia favus to almost 3.5 days net production in Sinularia dura (Table 3A).

(I’& and its share in produced

0.09 0.06

Alc~vonacea: L. venusturn Sinularia dura

Absolute values of mucus production the corals’ surface.

0.19 0.16 0.07 0.12

Fivia favus Favites pentagona P. daedalea G. interrupta

Scleractinia:

“; of daily

74P, 47?,

34”” 27”; 16% 21””

Rc without sediment

0.09 0.10

0.30 0.32 0.06 0.25

9 1 y/o 82%

65 “‘, 729, 1I 0% 53”/,

&with sediment

Y0 of daily

an unsedimented

0.21 0.12

0.17 0.80 0.60 0.40

Mucous sheet with sediment mg,Cgg’,d-’

conditions

1827, 338’j6

5670 300”/, 190% 141%

Mucous sheet, y0 of daily PC

sheet refers to the entire amount of mucus sticking to sediment removed from

86 ‘& 265 9;

177”; 1217” 19% 909,

“,,

PC with sediment

with scdimcnt mg.Cgg’.d-’

of daily

in sedimented

pM

(“,, 24 h Rc-) carbon

are given in mg C gcorai- 1 day - ‘. Mucous

58To 509;

33”/, 26% 14”; 2 7 ‘,

Of0of daily PC without sediment

without sediment mg.Cgg’.d-’

(“,, 24 h PC) or rcspircd

PM

Daily (24 h) mucus production

Table 3 Mucus production

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4. Discussion The results and the modelling exercise show the profound influence sediments exert on the energetic balance of symbiotic scleractinia and alcyonacea. This is partly due to absorbtion or reflection of light by the sediment, but also due to stimulation of mucus production. Both factors shift the coral’s energy balance, because of decreased photosynthesis by algae and of increased mucus losses. Both scleractinia and alcyonacea showed decreased photosynthesis and respiration in the presence of sediments. Alcyonacea showed little active behaviour to get rid of sediment, exept inflation of the entire corallum and the formation of mucous sheets (Riegl, 1995). The relative similarity of the different corals’ reactions, despite varying baseline production and respiration, allowed the construction of a generalized scheme of the physiological response to sedimentation. Fig. 3 is a conceptual diagram explaining the dynamics of sediment/coral interaction. It is based on the results from the 50% PARS model and the 25 y0 PARS model. The models assume a constant output of mucus over the day (Crossland et al., 1980). In normal conditions a high proportion of ambient light (vertical arrows) reaches the zooxanthellae (indicated as black dots), which photosynthetically produce carbon. Animal and algal respiration together accounted for about 90% of the daily net production. Of the total respiration approximately 35% was used for mucus production, while about 65% were free to be used for other metabolic requirements. Under the tested sedimentation conditions (200 mg . cmm2) the situation changed dramatically. Only about 25% of ambient light would have reached the zooxanthellae, which were thus able to photosynthesize only about half of the production reached under control conditions. Respiration accounted for about 130% of the daily production and 65 y0 of the total respiration was allocated to mucus production but only 35 % to general metabolic requirements. The increased respiration (relative to production) and the productivity loss due to reduction of light pushed the P/R ratios of all but one coral species (Lobophytum venustum) below 1, indicating a situation where photosynthesis produces less carbon than is respired. The fact that Lobophytum venustum still had a positive carbon balance can be explained by its growth form. Numerous high ridges on the coral’s upper surface create a large proportion of surface that cannot be covered by sediment and therefore did not suffer any losses in photosynthetic production. This emphasizes the importance of coral morphology as a counter to the harmful effects of sedimentation (Stafford-Smith, 1993; Riegl, 1995). In the 25% PARS model the energetic starting point for most corals was already in the heterotrophic domain, with P/R ratios well below 1 even under control conditions (Table 2). Again, as in the previous model, overall metabolic activity decreased with sediment application, while the proportional share of respiration in production doubled. In this model corals respired roughly 2.5 times the amount of carbon than they produced in 24 h. It is obvious that such a situation is unfavourable. Sedimentation not only interferes with the coral’s energy balance by forcing respiratory losses up and photosynthetic production down, it also reduces heterotrophic energy gain by interfering with the prey-capturing apparatus. This may be of lesser importance, as symbiotic corals were described as inefficient prey-catchers because of morphological adaptations to harbour

212

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Branch 1.J. Exp. Mar. Biol. Ecol. 186 11995) 259-275

50 % PARS without

light

sediment

“:

50 % PARS with

sediment

U=65

Rt=l

25 96 PARS wthout __~

30

light

sediment

25 % PARS wth

sediment

Fig. 3. Conceptual model of the influence of sediment on coral energy budgets. Semicircles symbolize corals, thin vertical arrows light, downward fat arrows are photosynthetic productivity (P, values are percentages of maximum production (lOO= lOOa<) in the unsedimented 50% PARS model; e.g. P = 50, under sedtment the coral has only 50% p roductivity compared to unsedimented conditions), outward directed horizontal arrows are total respiration (R,, expressed as percentage of the production inside the stylized coral, e.g. R, = 130 = total respiration used 1307; of daily productivity) indicating the share of respired C used for mucus production (M) and other energetic requirements (R). 0 symbolize zooxanthellae. Shading on the outside of semicircle indicates sediment.

zooxanthellae (Wilkinson et al., 1988). Under heavily sedimented conditions the corals therefore shut down most of their normal metabolic functions in order to produce large quantities of mucus, which aids sediment removal (Bak & Elgershuizen, 1976; Coffroth, 1988; Stafford-Smith & Ormond, 1992). The practice of producing mucous sheets (Coffroth, 1988; Stafford-Smith & Ormond, 1992) was an extremely costly way

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of reacting to the environment, as in most cases carbon equivalent to several days of production was released (Table 3). Over longer periods this is bound to create severe problems for the corals and may very well explain reported long-term changes in physiology (Szmant-Froelich et al., 1981) and damage to coral tissue by continued sedimentation (Peters & Pilson, 1985; Rogers, 1990; Stafford-Smith & Ormond, 1992). Modelling and mucus analysis showed that while the influence of sedimentation is comparable under different ambient light levels, corals living in lower light levels are more adversely affected than corals living in a better lit environment. The little available light gets even further reduced by sediments. The share of respiration (R,) in productivity (P) was found to be higher in poorly-lit than in better-lit conditions (Fig. 3). The 25% PARS model showed most corals to be heterotrophic over 24 h. The negative influence of sedimentation on energy uptake is more acute under low light levels. 5. Conclusion Sediments severely affected the energy budgets of all species investigated. Sediments caused a loss of available light, which led to decreased photosynthesis. A higher proportion of produced carbon was respired, resulting in P/R ratios lower than 1 in almost all species subject to either 50 or 25% PARS. Mucus production was an important carbon-sink. Under sediment stress, carbon requirements for stepped-up mucus production more than doubled. Mucus adhering to sediment was equivalent to photosynthetic production from one half to several days. Mucous sheets, commonly used by corals as defence against sedimentation, are metabolically very expensive. Acknowledgements Financial support by the South African Foundation for Research Development, the Endangered Wildlife Trust, the Department of National Education and the South African Association of Marine Biological Research is acknowledged with appreciation. M. Schleyer provided office space and laboratory equipment, J. Ballard helped with aquarium space and the transport of research corals. We also thank A.J. de Freitas, R.P. van der Elst, T. Kay, 0. Bourquin, W. Prinsloo, D. Durholtz and P. Cook for help in many ways. Y. Benayahu from Tel Aviv University kindly identified the soft corals. The insightful remarks of D. Barnes greatly improved the quality of the original manuscript. References Abdel-Salam, H. & J.W. Porter, 1988. Physiological effects of sediment rejection on photosynthesis and respiration in three Caribbean reef corals. Proc. 6th Int. Coral Reef Symp. Australia, Vol. 2, pp. 285-292. Bak, R.P.M. & J.H.B.W. Elgershuizen, 1976. Patterns of oil-sediment rejection in corals. Mar. Biob, Vol. 37, pp. 105-l 13. Beckley L.E. & R.C. van Ballegooyen, 1992. Oceanographic conditions during three ichthyoplankton surveys of the Agulhas current in 1990/91. S. Afr. J. Mar. Sci., Vol. 12, pp. 83-93.

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