Role of light intensity and spectral quality in coral settlement: Implications for depth-dependent settlement?1

Journal of Experimental Marine Biology and Ecology, 223 (1998) 235–255

L

Role of light intensity and spectral quality in coral settlement: Implications for depth-dependent settlement? 1 C.N. Mundy b

a ,c ,

*, R.C. Babcock b

a Australian Institute of Marine Science. PMB 3, Townsville MC, Qld 4810, Australia Leigh Marine Laboratory, University of Auckland, PO Box 349, Warkworth, New Zealand c Zoology Department, University of Queensland, Brisbane, Qld 4072, Australia

Received 21 November 1996; received in revised form 2 June 1997; accepted 23 June 1997

Abstract On coral reefs scleractinian corals show strong patterns of vertical zonation, yet the underlying mechanisms creating and maintaining vertical zonation are poorly understood. Here we examine the potential contribution of light-dependent settlement in scleractinian coral planulae to patterns of vertical zonation. The effect of intensity and spectral quality of light on the settlement of six species of scleractinian corals (Goniastrea favulus Dana, Goniastrea aspera Verrill, Acropora tenuis Dana, Oxypora lacera Verrill, Montipora peltiformis Bernard, and Platygyra daedalea Ellis and Solander) with contrasting depth distributions was examined in laboratory trials. Lightdependent settlement was shown by planulae from five of the six species examined. Planulae from individual species showed a response to either light quality or light quantity, but not both. Settlement patterns shown by planulae from all six species were consistent with the vertical distribution patterns of adults in the field. Settlement of planulae from con-generic species with similar adult distribution patterns did not respond to variation in light intensity or spectral quality in a uniform manner, indicating the optimal light environment for settlement is species specific. The settlement patterns shown by planulae from five of the six species examined were more complex than required for selection of cryptic or exposed micro-habitats at settlement. The ecological function of such complex responses to light at settlement may be to identify optimum habitats for adult survival.  1998 Elsevier Science B.V. Keywords: Coral; Larvae; Settlement; Behaviour; Light

*Corresponding author. Address for correspondence: Department of Conservation, PO Box 10-420 Wellington, New Zealand. Tel.: 1 644 471 3286; fax: 1 644 471 3279; e-mail: [email protected] 1 This is contribution number 872 from the Australian Institute of Marine Science. 0022-0981 / 98 / $19.00  1998 Elsevier Science B.V. All rights reserved. PII S0022-0981( 97 )00167-6

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1. Introduction Scleractinian corals show strong patterns of vertical zonation on both turbid inshore reefs (Bull, 1982), and offshore reefs bathed in oceanic waters (Done, 1982; Sheppard, 1982; Titlyanov and Latypov, 1991). Despite considerable research (more than 55 studies of patterns of coral zonation on Atlantic or Indo-Pacific reefs), the mechanisms underlying vertical zonation and the identity of physical factors that limit species distributions remain poorly understood (Sheppard, 1982; Done, 1983). Processes operating on adults clearly play major roles in determining the vertical distribution of some scleractinian corals (Sheppard, 1982; Chadwick, 1991; Done, 1992), as for other sessile marine invertebrates (Denley and Underwood, 1979; Witman, 1987; Menge, 1991). However, it is important to determine if larval behaviours prior to or at the time of settlement play comparable if not more important roles in this process (Grosberg and Levitan, 1992). Studies of natural recruitment to settlement plates deployed at several depths have reported shifts in orientation of coral recruits from lower to vertical and upper plate surfaces with increasing depth (Birkeland et al., 1981; Rogers et al., 1984; Wallace, 1985). This trend is assumed to result from light-dependent preferences of planulae at the time of settlement. Whether these observed patterns are a consequence primarily of light-dependent settlement or differential survival of settlers among plate surfaces with increasing depth is not yet clear (but see Babcock and Mundy, 1996). The importance of larval behaviour for determining adult depth distributions has been documented for intertidal barnacles (Denley and Underwood, 1979; Grosberg, 1982; Raimondi, 1988; Minchinton and Scheibling, 1991), and subtidal ascidians (Young and Chia, 1984; Stoner, 1992). However, there are few studies other than those for barnacles and ascidians that have examined the contribution of settlement patterns to the determination of depth distributions of subtidal sessile invertebrates. Due to the specialised nature of ascidian and barnacle larvae (e.g., large size, sensory capabilities, fast swimming), conclusions from these studies may not be generally applicable to subtidal sessile taxa (Keough and Downes, 1986). Many invertebrate larvae are known to display phototactic responses at some stage prior to settlement (Thorson, 1964). Ontogenetic shifts in photo- and geo-taxis have been observed for many sessile invertebrate larvae (e.g., barnacles – Lang et al., 1979; polychaetes – Marsden, 1988, 1990; Young and Chia, 1982; ascidians – Svane, 1987; Durante, 1991; molluscs – Kaartvedt et al., 1987; Barile et al., 1994; echinoderms – Pennington and Emlet, 1986; and crustaceans – Ritz, 1972; Sulkin and Van Heukelem, 1982; Forward, 1989; Olmi, 1994), and may either enhance or restrict dispersal. Preferences of invertebrate larvae for particular light intensities have also been shown to assist larvae to select particular microhabitats at the time of settlement (Weinberg, 1979; van Duyl et al., 1981; Hadfield, 1986; Svane and Young, 1989; Durante, 1991; Svane and Dolmer, 1995). Doyle (1974) found that slight differences in photo-responses of larvae from two populations of the polychaete Spirorbis borealis, were correlated with vertical distribution of the two populations and had a genetic basis. Miller and Hadfield (1986) suggest selective pressure for photo-responses may occur during both dispersal and settlement, although differentiation of photo-responses between these two phases has not always been clear.

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Light is an important environmental variable for reef building corals and is largely regarded as the factor limiting maximum depth of hermatypic coral growth (Falkowski et al., 1990). The intensity, spectral quality, and directional strength of light changes predictably with increasing depth (Falkowski et al., 1990; Kirk, 1994). The upper limits of growth of several scleractinians (e.g., Oxypora lacera) also decrease with increasing distance offshore, or increasing water clarity. On an inshore fringing reef in turbid conditions, the upper limit of O. lacera was 6–8 m (Babcock and Mundy, 1996), whereas on outer continental shelf reefs in clear oceanic waters O. lacera is rarely found above 20 m (pers. obs.). This suggests that the physical effect of depth (i.e. pressure) is not a limiting factor in the distribution of this species. Given the differences in light regime with increasing depth, the requirement of light for growth of hermatypic corals and that coral planulae show phototactic behaviour, the light field provides an ideal physical cue for coral planulae to locate optimal habitats for adult survival. Several previous studies have documented phototactic behaviour in coral planulae (Kawaguti, 1941; Lewis, 1974; Morse et al., 1988; Carlon and Olson, 1993; Babcock and Mundy, 1996). However, other than extreme differences in light intensity little is known of the extent to which planulae can perceive gradients in intensity and spectral quality, or directionality of the light field. Moreover, the ecological function of these phototactic behaviours in coral planulae is not clear. Non-selective settlement of coral planulae over a broad vertical range, would imply that vertical zonation is determined by factors (unknown) affecting post-settlement survival. Alternatively, selective settlement within depth strata implies a sensory capacity to discriminate between depth strata and an ability to influence vertical position within the water column. Coral planulae are unlikely to settle at random (Harrison and Wallace, 1990), although it has yet to be demonstrated that the behaviour of coral planulae contributes to more than fine-scale selection of micro-habitats. The mechanisms and cues by which coral planulae locate optimum depth strata and settlement sites for post-settlement survival, and the role of light intensity and particularly spectral quality in this process remain poorly understood. This study examines the potential contribution of light-dependent settlement in scleractinian coral planulae to patterns of vertical zonation. Specifically the effect of light intensity and spectral quality on settlement rate and on choice of upper (exposed) or lower (cryptic) plate surfaces at settlement were investigated.

2. Methods Settlement experiments were carried out at two sites on the central Great Barrier Reef (Geoffrey Bay, Magnetic Island (MI) and Pioneer Bay, Orpheus Island (OI)) during the annual summer spawning (Harrison et al., 1984; Babcock et al., 1986). We undertook additional experiments on Montipora spp during the minor spawning in March /April at Geoffrey Bay (Stobart et al., 1993). Coral species were chosen on the basis of vertical distribution patterns of adults. Species examined were either (1) restricted to shallow reef flat / crest habitats – Goniastrea favulus (MI, Oct. 1993), Goniastrea aspera (OI, 1994), Acropora tenuis (MI, Oct. 1994), (2) restricted to deep water or protected shaded habitats – Oxypora lacera (MI Oct. 1993, 1994, OI Nov. 1994); Montipora peltiformis (MI, Mar. 1994), or (3) distributed over a broad depth range, occurring in both deep and

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shallow reef habitats – Platygyra daedalea (OI, Nov. 1994). Depth distributions of these species have been documented in several previous studies (Babcock, 1984; Veron, 1986; Titlyanov and Latypov, 1991; Stobart et al., 1993; Miller, 1994; Babcock and Mundy, 1996; Mundy, 1996).

2.1. Larval culture Eight to 10 mature colonies of each target species were collected during the afternoon of the day of spawning and placed in large plastic containers on the shore. Naturally spawned gametes were collected and transferred to 2.5 l plastic jars. A large diameter hole in the lid was covered with 105 or 210 mm plankton mesh to allow water exchange. The jars containing coral embryos were then attached to a rope anchored on the reef slope for approximately 4 days, to allow development of planulae under ambient temperature and salinity conditions (see Babcock, 1985). Fresh seawater was flushed through the jars two to three times per day.

2.2. Settlement experiments: equipment and procedure Coral planulae were transferred from the reef to the laboratory at the Australian Institute of Marine Science (AIMS) on all occasions except during the offshore coral spawning at Orpheus Island in November / December 1994 where experiments were carried out at the Orpheus Island Research Station. All experiments were located in outside aquaria, using natural light and commercially available theatrical light filters (Lee) of differing colour and intensity. The ceilings of outdoor aquaria structures were covered with 50% shade cloth, providing more diffuse and less intense lighting, and prevented overheating of aquaria (with the exception of experiments involving Montipora peltiformis in March 1994, when aquaria were exposed to full sunlight). The experimental setup consisted of large opaque PVC trays (400 mm 3 270 mm 3 150 mm), each of which contained two smaller trays with open side panels covered by 210 mm plankton mesh. The filter medium was embedded in a sheet of heavy black plastic (600 mm 3 400 mm) and placed over the large tray, such that the only light entering the tray, and inner boxes was that passing through the light filter. The bottom of the large tray was covered with 70% black shade cloth to reduce upward reflection. A single settlement plate (110 mm 3 110 mm 3 10 mm terracotta tile) was placed in each inner tray and raised 10 mm from the floor of the tray. Upper and lower surfaces of tiles were flat but with numerous grooves and pits in the tile surface (up to 1 mm deep) which were produced during the manufacturing process. The tile edges however, were relatively smooth with no indentations. Settlement plates were conditioned in outdoor aquaria for at least three weeks prior to settlement experiments. The large trays were supplied with unfiltered fresh seawater. Five light treatments were used in these experiments: (1) high light intensity neutral density filter (Hneut); (2) medium light intensity neutral density filter (Mneut); (3) medium light intensity blue filter (Mblue); (4) low light intensity neutral density filter (Lneut); and (5) low light intensity blue filter (Lblue). Percent transmission of incident light for the five filter treatments are shown in Table 1.

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Table 1 Percent transmission of visible wavelengths (400–700 nm) through filter medium (max intensity recorded was 1240 mE m 22 s 21 )

% Transmission

Hneut

Mblue

Mneut

Lblue

Lneut

74.80

51.03

40.30

14.55

11.46

The filter treatments were chosen to simulate total irradiance (1000–100 mE m 22 s 21 ) and spectral quality observed at a range of depths in previous studies (Brakel, 1979; Dustan, 1982; Babcock and Mundy, 1996). The neutral density filters (Hneut, Mneut, Lneut) lower total irradiance while retaining the spectral composition of incident light at the sea surface. The blue filters (Mblue, Lblue) reproduce the spectral composition of light at depth (i.e. greater attenuation of red wavelengths) in addition to lowering total irradiance. The medium and low intensity blue filters (Mblue and Lblue) provide similar spectral composition and intensity to that recorded at 5 and 20 m, respectively, by Dustan (1982). The reduction in light intensity provided by medium and low light intensity filters is also within the range recorded by Babcock and Mundy (1996) at the mid and lower slope at Geoffrey Bay, Magnetic Island. Percentage transmission of individual wavelengths (350 to 700 nm) for the five filter treatments were obtained by scanning filter sections with a spectrophotometer (1 nm intervals), and are shown in Fig. 1. The density of planulae in the 2.5 l rearing jars was determined by mixing the larval culture within each pot thoroughly and counting planulae in replicate 10 ml aliquots. The appropriate volume of culture was then added to each inner tray to achieve a concentration of 1000 planulae per inner tray. Each tray contained planulae from only one species. Planulae were added to the trays when the planulae were 4–5 days old, and the majority of planulae in the culture would be competent to settle (Babcock and Heyward, 1986). Experiments with planulae from Goniastrea favulus, Acropora tenuis, Oxypora lacera (Magnetic Island 1994), and Platygyra daedalea included all five light treatments, with four replicate plates in each treatment. Replicate plates for each species

Fig. 1. Percentage transmittance of wavelengths between 350 and 700 nm through light filters used in settlement experiments. (Hneut – high intensity, neutral filter; Mneut – medium intensity, neutral filter; Lneut – low intensity, neutral filter; Mblue – medium intensity, blue filter; Lblue – low intensity, blue filter).

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by light treatment combination were located in separate trays. Insufficient planulae of G. aspera, Montipora peltiformis and O. lacera (Magnetic Island 1993, Orpheus Island 1994) were obtained to include all five light treatments. In these experiments, fewer light treatments were used but the number of planulae per experimental unit and number of replicates per treatment were as for all other experiments. Most planulae had either settled or ceased swimming 5 days after the experiment was commenced (age of planulae 9–10 days). At this time, settlement plates were examined in a shallow water bath using a dissecting microscope. The number of settled and metamorphosed planulae on the upper surface, side, and lower surface of each plate was recorded. Only those planulae which were securely attached, and had reached the flattened disk stage described by Harrison and Wallace (1990), page 191, were considered to have settled and metamorphosed.

2.3. Data analysis The effect of light treatments on settlement of planulae was examined using a two factor split-plot ANOVA. The main effects are ‘‘Light’’ with five levels, ‘‘Surface’’ with three levels, and ‘‘Plate nested within Light’’. This design provides tests for significant differences in settlement among (a) light treatments (b) plate surfaces, and (c) the presence of a light by surface interaction. Statistical analyses were performed separately for each species. The treatments within the ‘‘Light’’ effect were, (1) high intensity– neutral density (Hneut), (2) medium intensity–neutral density (Mneut), (3) low intensity–neutral density (Lneut), (4) medium intensity–blue (Mblue), and (5) low intensity–blue (Lblue). Treatments within plate surface were upper (121 cm 2 ), vertical (plate edge; 40 cm 2 ), and lower plate surfaces (121 cm 2 ). Data were analysed as number of settlers per 100 cm 2 (density) to standardise settlement rate among plate surfaces. Analyses of Goniastrea favulus and Oxypora lacera (MI 1993) had only two plate surface treatments (upper and lower). Given that vertical distribution patterns of adults were known a priori, planned comparisons were used to test for differences in settlement among light treatments. For species where data from all five light treatments were obtained the planned comparisons were: H0:

1

H0:

2

H0:

3

H0:

4

Hneut vs. Lneut to test for effect of different light intensity on settlement density, keeping spectral composition constant; Hneut vs. Lblue to test for differences in settlement density between shallow and deep light environments; Lneut vs. Lblue to test for effect of spectral composition keeping intensity constant – at low light intensity; Mneut vs. Mblue to test for effect of spectral composition keeping intensity constant – at medium light intensity.

Settlement experiments involving Montipora peltiformis and Oxypora lacera (Magnetic Island 1993) included only Hneut, Lneut, and Lblue. Experiments with Goniastrea

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241

aspera and O. lacera (Orpheus Island 1994) used Hneut, Mneut and Lblue. Planned comparisons for M. peltiformis and O. lacera (MI 1993) were: H0:

1

H0:

2

Hneut vs. Lneut to test for effect of different light intensity on settlement density, keeping spectral composition constant; Lneut vs. Lblue to test for effect of spectral composition keeping intensity constant – at low light intensity,

while for G. aspera and O. lacera (OI 1994) the planned comparisons were: H0:

1

H0:

2

Hneut vs. Lblue to test for differences in settlement density between shallow and deep light environments; Hneut vs. reduced light treatments (Mneut 1 Lblue) for G. aspera and, Lblue vs high light intensity treatments (Hneut 1 Mneut) for O. lacera (OI 1994).

The planned comparisons described above were not orthogonal, therefore critical values used in significance tests were adjusted using the Dunn–Sidak method to control the experiment-wise error rate (Sokal and Rohlf, 1981, p. 242). Interesting features suggested by post hoc examination of means were examined using the T method (Tukeys Honestly Significant Difference) (Sokal and Rohlf, 1981).

3. Results The proportion of planulae settled on plates (light treatment and plate surface pooled) varied considerably among species. The highest settlement rates observed were by Acropora tenuis planulae (35.6% of planulae added) and the lowest settlement rate by Montipora peltiformis planulae (1.4% of planulae added). A significant interaction between light and plate surface was found for four of the six species examined (M. peltiformis, Acropora tenuis, Oxypora lacera (MI and OI in 1994) and Platygyra daedalea), indicating that the choice of plate surface at settlement by planulae of these species was dependent on ambient light. Detailed results for each species are presented in the following sections.

3.1. Settlement response of reef flat /crest species A significant effect of light treatment on settlement density was found for the reef flat species Goniastrea favulus, as indicated by the significant planned comparison of low light intensity neutral density vs. low light intensity blue (a 5 0.05, Table 2). Fig. 2(a) shows settlement of G. favulus was significantly lower under the low light blue treatment than the low light neutral treatment. Settlement of G. favulus planulae did not vary significantly between upper and lower plate surfaces (Table 2, Fig. 2(b)). Settlement rate of Goniastrea aspera did not differ statistically among light treatments at a 5 0.05, (although significant at a 5 0.1, Table 2), despite the average settlement density under the high intensity neutral treatment (Hneut) being more than twice that

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Table 2 Results of two factor split-plot ANOVA on settlement response to experimental manipulation of light for three reef flat / crest species, Goniastrea favulus, Acropora tenuis and Goniastrea aspera Goniastrea favulus

Source

df

F

p

Light Hneut vs. Lneut Hneut vs. Lblue Lneut vs. Lblue Mneut vs. Mblue Rep (Light) 5 Error 1 Side Light 3 Side Error 2

4 1 1 1 1 15 1 4 15

2.8 0.79 3.89 8.18 2.20

ns

0.87 1.43

0.37 0.27

Light Hneut vs. Lblue Hneut vs. (Mn 1 Lb) Rep(Light) 5 Error 1 Side Light 3 Side Error 2

2 1 1 9 2 4 18

3.01 2.89 5.55

0.10 ns ns

8.37 1.73

0.01 0.19

Light Hneut vs. Lneut Hneut vs. Lblue Lneut vs. Lblue Mneut vs. Mblue Rep(Light) 5 Error 1 Side Light 3 Side Error 2

4 1 1 1 1 13 2 8 26

3.55 8.33 10.78 0.02 0.48

0.04 ns ns ns

94.43 8.7

0.001 0.001

0.06 ns ns a

Goniastrea aspera

Acropora tenuis

a

a

p , 0.05. Light treatments were Hneut 5 high light neutral density filter; Mneut 5 medium light intensity neutral density filter; Lneut 5 low light intensity neutral density filter; Mblue 5 medium light intensity blue filter; Lblue 5 low light intensity blue filter.

observed in either the medium intensity neutral (Mneut) or low intensity blue (Lblue) treatments (Fig. 3(a)). However, settlement of G. aspera planulae was significantly higher on upper plate surfaces than either vertical or lower plate surfaces (Tukeys HSD, df 5 18, a 5 0.05; Fig. 3(b)). Settlement density of Acropora tenuis was dependent on both light treatment and plate surface, as indicated by significant interaction (Table 2), with differences in settlement density between plate surfaces decreasing with decreasing light intensity (Fig. 4). Overall settlement was highest under the high light neutral treatment (Hneut), and declined gradually with decreasing light intensity to a low under the low light neutral treatment (Lneut, Fig. 4(b)). Settlement density was also substantially higher on vertical plate sides than either upper or lower plate surfaces in all light treatments (Fig. 4(b)). Settlement density of A. tenuis on upper plate surfaces showed a similar decline to that

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Fig. 2. Settlement density of Goniastrea favulus planulae in five light treatments (Hn 5 high neutral; Mb 5 medium blue; Mn 5 medium neutral; Lb 5 low blue; Ln 5 low neutral). Data shown are (a) mean settlement density – plate surfaces pooled, and (b) mean settlement density by surface and light treatment. Error bars indicate standard errors. Light treatments arranged from left to right by decreasing level of light intensity.

observed on the vertical plate sides, although the differences in settlement density between the extremes of Hneut and Lneut were considerably less (Fig. 4(b)). The pattern of decline in mean settlement rate of A. tenuis with decreasing total irradiance, differed from the pattern observed for Goniastrea favulus, where no such trend was evident (Fig. 2). Settlement response of the shallow reef corals Goniastrea favulus, Acropora tenuis, and G. aspera to the experimental light treatments were consistent with their adult

Fig. 3. Settlement density of Goniastrea aspera planulae in three light treatments (Hn 5 high neutral; Mn 5 medium neutral; Lb 5 low blue). Data shown are (a) mean settlement density – plate surfaces pooled, and (b) mean settlement density by surface and light treatment. Error bars indicate standard errors. Light treatments arranged from left to right by decreasing level of light intensity. Note: different scales on y axis.

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Fig. 4. Settlement density of Acropora tenuis planulae in five light treatments (Hn 5 high neutral; Mb 5 medium blue; Mn 5 medium neutral; Lb 5 low blue; Ln 5 low neutral). Data shown are (a) mean settlement density – plate surfaces pooled, and (b) mean settlement density by surface and light treatment. Error bars indicate standard errors. Light treatments arranged from left to right by decreasing level of light intensity. Note: different scales on y axis.

distribution patterns. Settlement of planulae from the reef flat species G. favulus was only reduced when both light intensity and spectral composition reflected light regime of deep water habitats. In contrast to G. favulus, A. tenuis and G. aspera planulae showed a reduction in settlement with a reduction in light intensity, irrespective of spectral composition.

3.2. Settlement response of lower slope species Patterns of settlement from the three experiments involving the deep slope species Oxypora lacera were similar overall. However, in the 1994 experiments at both Magnetic and Orpheus Islands, a significant interaction was found between light treatment and plate surface (Table 3). In the 1993 experiment with O. lacera planulae from Magnetic Island, settlement was significantly higher in the low intensity neutral treatment (Lneut) than the high intensity neutral treatment (Hneut) (Table 3, Fig. 5(a)). Settlement density was also significantly higher on lower plate surfaces than on upper plate surfaces (Table 3, Fig. 5(b)). In 1994 at Magnetic Island, settlement density was low under all light treatment, plate surface combinations, except for settlement density on upper plate surfaces in the two low light treatments Lblue and Lneut (Fig. 6). A similar pattern was found for the Orpheus Island experiment, where settlement was again low under all treatment combinations with the exception of settlement on the upper plate surface in the low light blue treatment (Lblue, Fig. 7). Settlement density of Montipora peltiformis was also dependent on both light treatment and plate surface (Table 3). Settlement density was low on all surfaces under both extremes of light intensity (Hneut and Lneut) and on the upper plate surface in the

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Table 3 Results of two factor split-plot ANOVA on settlement response to experimental manipulation of light for two lower reef slope species Oxypora lacera and Montipora peltiformis Oxypora lacera

Source

Magnetic Island 1993

Light Hneut vs. Lneut Lneut vs. Lblue Rep(Light) 5 Error 1 Side Light 3 Side Error 2

Oxypora lacera Magnetic Island 1994

Oxypora lacera Orpheus Island 1994

df

F

p

2 1 1 8 1 2 8

6.35 11.95 7.24

0.02

9.17 0.08

0.016 0.926

Light Hneut vs. Lneut Hneut vs. Lblue Lneut vs. Lblue Mneut vs. Mblue Rep(Light) 5 Error 1 Side Light 3 Side Error 2

4 1 1 1 1 10 2 8 20

12.78 13.96 42.04 1.38 2.75

ns ns

12.49 8.64

0.001 0.001

Light Hneut vs. Lblue Lblue vs. (Cl 1 Mn) Rep(Light) 5 Error 1 Side Light 3 Side Error 2

2 1 1 9 2 4 18

8.37 5.93 14.09

0.01 ns

23.76 11.77

0.001 0.001

Light Hneut vs. Lneut Lneut vs. Lblue Rep(Light) 5 Error 1 Side Light 3 Side Error 2

2 1 1 8 2 4 16

9.05 0.45 11.64

0.01 ns

a

ns

0.001 a c

b

Montipora peltiformis

7.53 4.86

a

0.01 0.01

a

p , 0.05. p , 0.01. c p , 0.001. Experiments involving O. lacera were carried out on three occasions using planulae obtained from Magnetic Island in 1993 and 1994, and from Orpheus Island in 1994. Light treatments were Hneut 5 high light neutral density filter; Mneut 5 medium light intensity neutral density filter; Lneut 5 low light intensity neutral density filter; Mblue 5 medium light intensity blue filter; Lblue 5 low light intensity blue filter. b

low light blue treatment (Lblue), however settlement increased on vertical plate sides and lower plate surfaces in the low light blue treatment (Fig. 8). Settlement responses of planulae from the lower slope species Oxypora lacera and Montipora peltiformis planulae were consistent with adult distribution patterns in the

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Fig. 5. Settlement density of Oxypora lacera (Magnetic Island 1993) planulae in three light treatments (Hn 5 high neutral; Lb 5 low blue; Ln 5 low neutral). Data shown are (a) mean settlement density – plate surfaces pooled, and (b) mean settlement density by surface and light treatment. Error bars indicate standard errors. Light treatments arranged from left to right by decreasing level of light intensity.

field. Settlement rate of O. lacera planulae increased with decreasing light intensity, irrespective of spectral composition. In contrast, settlement of M. peltiformis planulae only increased when both light intensity and light quality simulated light conditions in deep water habitats.

Fig. 6. Settlement density of Oxypora lacera (Magnetic Island 1994) planulae in five light treatments (Hn 5 high neutral; Mb 5 medium blue; Mn 5 medium neutral; Lb 5 low blue; Ln 5 low neutral). Data shown are (a) mean settlement density – plate surfaces pooled, and (b) mean settlement density by surface and light treatment. Error bars indicate standard errors. Light treatments arranged from left to right by decreasing level of light intensity. Note: different scales on y axis.

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Fig. 7. Settlement density of Oxypora lacera (Orpheus Island 1994) planulae in three light treatments (Hn 5 high neutral; Mn 5 medium neutral; Lb 5 low blue). Data shown are (a) mean settlement density – plate surfaces pooled, and (b) mean settlement density by surface and light treatment. Error bars indicate standard errors. Light treatments arranged from left to right by decreasing level of light intensity. Note: different scales on y axis.

3.3. Settlement response of ubiquitous species Underlying the apparently uniform settlement of Platygyra daedalea among light treatments (Fig. 9(a)) were considerable differences in settlement among plate surfaces,

Fig. 8. Settlement density of Montipora peltiformis planulae in three light treatments (Hn 5 high neutral; Lb 5 low blue; Ln 5 low neutral). Data shown are (a) mean settlement density – plate surfaces pooled, and (b) mean settlement density by surface and light treatment. Error bars indicate standard errors. Light treatments arranged from left to right by decreasing level of light intensity.

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Fig. 9. Settlement density of Platygyra daedalea planulae in five light treatments (Hn 5 high neutral; Mb 5 medium blue; Mn 5 medium neutral; Lb 5 low blue; Ln 5 low neutral). Data shown are (a) mean settlement density – plate surfaces pooled, and (b) mean settlement density by surface and light treatment. Error bars indicate standard errors. Light treatments arranged from left to right by decreasing level of light intensity. Note: different scales on y axis.

as indicated by the significant interaction between plate surface and light treatment (Table 4). The density of P. daedalea settlers shifted from being predominantly on lower plate surfaces under the high light neutral treatment (Hneut), to upper plate surfaces as the light intensity of treatments increased (Fig. 9(b)). Settlement of P. daedalea planulae was very low on vertical plate sides under all light treatments (Fig. 9(b)). The similar overall settlement density of P. daedalea planulae under the five light treatments is consistent with the broad vertical distribution of adult P. daedalea observed in the field, although preference for cryptic vs. exposed habitats at settlement clearly varied in response to light intensity.

Table 4 Results of two factor split-plot ANOVA on settlement response to experimental manipulation of light for the ubiquitous species Platygyra daedalea Platygyra daedalea

Source

df

Light Hneut vs. Lneut Hneut vs. Lblue Lneut vs. Lblue Mneut vs. Mblue Rep(Light) 5 Error 1 Side Light 3 Side Error 2

4 1 1 1 1 15 2 8 30

F

p

0.75 1.32 1.00 0.02 0.98

0.57 ns ns ns ns

11.62 2.6

0.00 0.03

Light treatments were Hneut 5 high light neutral density filter; Mneut 5 medium light intensity neutral density filter; Lneut 5 low light intensity neutral density filter; Mblue 5 medium light intensity blue filter; Lblue 5 low light intensity blue filter.

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4. Discussion The results obtained from experiments detailed here show phototactic responses of coral planulae are not limited to simple recognition of light / dark extremes. For planulae of some coral species, the spectral composition of the light environment is clearly as important as light intensity for settlement and metamorphosis (e.g., Goniastrea favulus, Fig. 2, and Montipora peltiformis, Fig. 8). Additionally, settlement of coral planulae may not be linearly related to either intensity or spectral quality. The settlement patterns of planulae in relation to light are consistent with the vertical distribution patterns in the field of adults from all six species examined. Settlement of planulae from the reef flat / crest corals Goniastrea aspera and Acropora tenuis were highest under the high light intensity neutral treatment (Hneut), and lowest under the low light intensity blue treatment (Lblue) which simulates lower slope light environments (Figs. 3 and 4). Settlement of planulae from the reef flat coral G. favulus was higher under all treatments with shallow water spectral compositions (Hneut, Mneut, Lneut) irrespective of irradiance level, but significantly lower under the low intensity blue treatment Lblue (Table 2, Fig. 2). In contrast to the shallow species, settlement of the lower slope species Oxypora lacera and Montipora peltiformis was highest under the low light intensity blue treatment Lblue which simulates lower slope light regimes, and lowest under the high light intensity neutral treatment Hneut, which simulates shallow water light regimes (Figs. 5–8). The response shown by Platygyra daedalea planulae differed from all other species examined, in that the overall settlement density was indifferent to light intensity and spectral composition (Fig. 9(a)), which is consistent with the broad vertical distribution of this species in the field (Miller, 1994; Mundy, 1996). Planulae from the con-generic corals Goniastrea favulus and G. aspera which have similar adult distribution patterns (restricted to shallow reef flat habitats) showed contrasting responses to variation in intensity and spectral quality of light. Settlement density of G. favulus decreased in response to a shift from shallow water light spectra to deep water light spectra, but not with a decrease in light intensity from 90 to 10%. In contrast, settlement density of G. aspera decreased in response to decreasing light intensity, but was independent of spectral quality. These results indicate that optimal light environment for settlement of coral planulae could be species specific. Moreover, species in the same genus with similar vertical distributions cannot be assumed to respond in a similar manner. The large differences in settlement density among light treatments by individual species and differences among species has important implications for studies investigating other factors potentially affecting settlement of corals. Investigation of factors such as substratum cues, presence / absence of competitors, or investigations of minimum times to settlement may be influenced significantly by light conditions provided in experimental manipulations. Many reports in the literature of minimum times to settlement for brooded planulae (summarised in Fadlallah, 1983; Harrison and Wallace, 1990) may have over estimated the time required before settlement or metamorphosis, particularly if light conditions provided in experimental aquaria were sub-optimal. How planulae respond to simultaneous variation in multiple cues / factors (e.g., light, biotic cues, sedimentation) is currently unknown (but see Morse et al., 1988).

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Preferences for different plate surfaces also varied considerably among species in this study, with four species displaying shifts in preference for a particular surface in response to increasing / decreasing light intensity. Few planulae of Goniastrea aspera or Platygyra daedalea settled on vertical plate sides under all light treatments (Figs. 3 and 9). This appeared to be in response to a preference for cryptic settlement sites by these planulae (positive thigmotaxis). Planulae of P. daedalea and G. aspera were observed to preferentially settle in grooves and indentations (approximately 1mm deep), particularly under the high and medium light intensity treatments of Hneut, Mneut and Mblue. The upper and lower plate surfaces of terracotta tiles used in this study contained numerous grooves and indentations, whereas the vertical plate sides had none. G. aspera planulae also preferred the upper plate surface in all light treatments (Fig. 3). In contrast to G. aspera and P. daedalea, greater numbers of Acropora tenuis planulae settled on vertical plate sides than either the upper or lower plate surface (Fig. 4). Planulae of both A. tenuis and Oxypora lacera are larger than those of P. daedalea and G. aspera (Babcock et al., 1986) and tended to settle on open flat surfaces and did not preferentially settle in crevices or indentations (pers. obs.). The three experiments involving Oxypora lacera planulae showed similar overall trends among light treatments (Figs. 5–7). In all cases settlement was reduced under high light levels. Settlement orientation was likewise consistent among the three experiments, with a trend of increasing settlement on upper surfaces as available light decreased. This trend in settlement orientation with decreasing light levels parallels that reported for O. lacera by Babcock and Mundy (1996). These authors however found no reduction in total settlement with decreasing light intensity either in field or aquarium experiments. In the case of Babcock and Mundy’s aquarium results, this apparent conflict may be related to the low levels of light available in their low light treatments (6 mE m 22 s 21 as apposed to 100–80 mE m 22 s 21 in the low light treatments used here). The range of values employed by Babcock and Mundy in their field experiments with O. lacera ranged from 1000–400 mE m 22 s 21 , equivalent to high and medium treatments in this study (Table 1). Differences in experimental procedures must be considered, but these results suggest a settlement optimum between 400 and 100 mE m 22 s 21 for O. lacera planulae. The presence of light-dependent settlement on plate surfaces in this study supports suggestions in earlier studies (Birkeland et al., 1981; Rogers et al., 1984; Wallace, 1985) that orientation of natural recruits on artificial settlement substrata is a consequence of light-dependent settlement behaviour. Babcock and Mundy (1996) also found lightdependent selection of settlement plate surface in the field and in laboratory aquaria, in the absence of confounding factors such as sediment, grazing or biotic cues. However, the ecological function of such behaviour in planulae of species with restricted depth distributions is unclear, and may only benefit species which occur over large depth ranges, such as Platygyra daedalea.

4.1. Implications for settlement processes in scleractinian corals The results obtained in this study provide additional evidence for the importance of light in the settlement process of scleractinian coral planulae. An ability of planulae to recognise extremes in light intensity (Kawaguti, 1941; Lewis, 1974) or discriminate

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between shaded and unshaded surfaces (Morse et al., 1988) would be sufficient to enable planulae to choose between cryptic and exposed micro-habitats at settlement. If selection of microhabitat at settlement was the only function of photo-response in coral planulae then settlement patterns of corals under different light treatments should parallel the patterns shown by Platygyra daedalea in this study and of P. sinensis reported in Babcock and Mundy (1996) (i.e. light-dependent selection of exposed / cryptic surface, but no effect on overall settlement density). However, settlement densities of species examined in this study, with the exception of P. daedalea, differed from this model. Additionally, settlement density of Goniastrea favulus and Montipora peltiformis planulae only changed when spectral quality was altered in addition to light intensity. Parallels between the field distribution patterns of adults and settlement patterns shown by all species examined suggest planulae of these species use light to locate or recognise optimum depths for settlement. Behavioural traits such as this which increase the probability of juvenile or adult survivorship would clearly be adaptive (Young and Chia, 1984; Carlon and Olson, 1993). Confirmation of the use of cues by coral planulae to locate particular depth strata at settlement requires demonstration of stratification of planulae in the water column (e.g., Grosberg, 1982), or differential settlement of species with depth in the field (e.g., Stoner, 1992). Given the difficulty of determining the specific identity of coral planulae or recent settlers on the basis of morphological characters, this maybe an impossible task. Planulae of some scleractinian species (e.g., Pocillopora damicornis) have sufficient identifying characters which in addition to time of release during the lunar phase enable them to be distinguished from planulae of several other species (Hodgson, 1985a), at least in low diversity systems. However, plankton samples taken from several depths in Kaneohe Bay gave inconclusive evidence concerning the stratification of P. damicornis planulae in the water column (Hodgson, 1985b). Coral planulae were previously considered as ‘‘passive meroplanktonic larvae’’ (Harrison and Wallace, 1990), contributing to an implicit assumption that coral planulae settle over a wide depth range. Hodgson (1985b) measured the swimming speed of Pocillopora damicornis planulae at up to 15 cm min 21 in aquaria. Slightly lower swimming speeds have been recorded for two other scleractinians, Acropora millepora (7.8 cm min 21 ) and Oxypora lacera (9.0 cm min 21 ), also in aquarium experiments (RCB unpublished data). This places the swimming speed of planulae from these species within the range of swimming speeds of micro- and mezo-holozooplankton known to perform vertical migrations (Mileikovsky, 1973). Furthermore, benthic marine invertebrate larvae capable of swimming speeds in excess of 1 cm min 21 have been shown to perform some active vertical movement irrespective of tidal currents (Mileikovsky, 1973). Thus swimming speeds of coral planulae, in concert with an ability to recognise differences in shallow and deep light regimes, may enable them to select a depth within the water column where they are most likely to encounter substratum at a depth optimal for post-settlement survival. Behaviour of planulae at the time of settlement that acts to concentrate settlers in habitats where post-settlement survival is optimal is considered to be an adaptive response to ‘‘strong sources of mortality acting differentially in space’’ (Young and Chia, 1984). We interpret the apparent preference of planulae for particular light regimes at settlement in five of the six species examined here as adaptive behavioural responses

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to strong selective pressure. Selective pressure resulting in larval preference for particular light regimes at settlement may operate at any age from recent settlers to reproductive adults. However, the identity of selective forces responsible for the observed settlement behaviours are unknown (Done, 1982; Sheppard, 1982; Falkowski et al., 1990). Recent reports (Mundy, 1996; Babcock and Mundy, 1996) indicate that for at least three of the species studied here, Oxypora lacera, Platygyra daedalea, Goniastrea aspera, as well as P. sinensis, juvenile mortality with depth is not consistent with adult depth distributions. Bak and Engel (1979) reported that species composition of juveniles was identical to adult distribution patterns at a range of depths. If adult distribution is not determined by post-settlement mortality, as indicated in these reports, larval behaviour before and at settlement may be a primary factor in establishing depth distributions of coral species. That many reef building coral species show similar restricted depth distributions on many reefs (Done, 1982) implies widespread selective pressure does exist for larval behaviour which concentrates settlers at favourable depths. Whether coral planulae use light cues to alter their position in the water column prior to reaching the substratum, or to initiate substratum selection behaviour or continue swimming after the substratum is encountered, was not examined in the experiments described here. With the exception of Platygyra daedalea, a significant proportion of planulae clearly chose not to settle in one or more light treatments, suggesting light conditions in those treatments were unsuitable or, light conditions did not provide the appropriate stimulus for settlement. In the field, if planulae encounter the substratum at sub-optimal depths, planulae may postpone substratum selection behaviour, and continue swimming until an acceptable light field is encountered. An alternative, but not mutually exclusive, model is that planulae in the water column change direction of swimming or buoyancy in response to intensity, quality or directionality of light in order to maximise the chance of encountering the substratum at optimal depths for post-settlement survival. This type of photo-response by planulae would be highly advantageous in species where adults occur within a restricted depth range. We suggest that the ecological function of light-dependent settlement in planulae from some coral species is to locate optimum depths for adult survival, rather than to merely differentiate between cryptic and exposed microhabitats. Acknowledgements We thank K. Miller, U. Siebeck, E. Turak, B. Stobart, and P. Harrison for assistance in the field. Andy Davis and two anonymous reviewers provided useful comments on a draft of this manuscript. This research was supported financially by an Australian Institute of Marine Science Postgraduate Research Award (to C.N.M.), the Zoology Department, University of Queensland, and by Great Barrier Reef Marine Park Authority Augmentative Grants (to C.N.M.). References Babcock, R.C., 1984. Reproduction and distribution of two species of Goniastrea (Scleractinia) from the Great Barrier Reef Province. Coral Reefs 2, 187–195.

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