Indian Journal of Marine Sciences Vol. 39(2), June 2010, pp. 219-226

Observations on the reproduction of along the Tuticorin coast of the Gulf of Mannar, Southeastern

K Diraviya Raj & J K Patterson Edward Suganthi Devadason Marine Research Institute, 44-Beach Road, Tuticorin–628 001, Tamil Nadu, India [E-mail: [email protected]] Received 5 February 2009; revised 22 June 2009

Pattern of reproduction was studied in Acropora species along Tuticorin coast in the Gulf of Mannar from 2006-2008. Extensive surveys were conducted to monitor reproductive maturity and the timing of spawning. Gametes were observed from January with colonies releasing gametes by the end of March. Acropora cytherea showed immature colonies in January (48-79%) and February (56-76%) and mature colonies in March (36-86%). Likewise, the other species of Acropora examined showed 50-75% of immature colonies in January and an increase of 10-20% of immature colonies in February, and matured in March. The average percentage of mature colonies in March was as follows, A. formosa 47-76%, A. valenciennesi 50-81%, A. intermedia 50-81%, A. nobilis 25-82%, A. micropthalma 56-83%, A. hemprichi 39-83%, A. hyacinthus 33-100%, A. corymbosa 59-65%. Spawning was observed in A. cytherea on 24 March 2006, 10 days after full moon; 28 March in 2007, 5 days prior to full moon; and 8 March 2008, 1 day after new moon. Approximately 30,000 egg and sperm bundles were observed in 1 litre of water and each bundle had 20-25 eggs in A. cytherea . Environmental parameters, especially rise in temperature at the end of March was believed to play lead role in spawning.

[Keywords: Acropora , Spawning, Immature, Mature, Reproduction]

Introduction the southern end of the Gulf of Mannar Marine The life cycle of corals includes a free-living National Park. Different types such as platform, planktonic planula phase and a sessile phase, and patch and fringing type are observed in the Gulf of various asexual and sexual modes of reproduction. Mannar. The islands have dominantly fringing reefs Spawning to the process in which corals release sperm and also patch reefs around them. Narrow fringing and eggs to be fertilized externally 1. Sexual reproduction reefs are located mostly at a distance of 50 to 100 m in corals involves the process of gametogenesis, which from the islands. On the other hand, patch reefs rise may require from a few weeks to over 10 months 2. Coral from depths of 2 to 9 m and extend to 1 to 2 km in spawning and reproduction allow corals to inhibit other length with width as much as 50 m. Reef flats are geographic areas and recover from damage of stressful extensive in almost all the reefs in the Gulf of Mannar. events. During their larval stage, corals can travel longer Reef areas of the Tuticorin coast in the Gulf of distances and can eventually settle on reefs quite far Mannar have been severely damaged due to from where were spawned 3. anthropogenic activities, in particular coral mining, With reef degradation and destruction occurring on a dynamiting and other destructive practices, and hence it global scale 4, an application of the reproductive data is is important to have a basic data base on the coral necessary in the area of reef restoration. Even though reproduction in this area. In India, the study on coral sexual reproduction is one of the most important reproductive biology is new to science and this study is processes for the persistence of reefs, little is known first such effort. Reproductive maturity of the Acropora about the factors that regulate reproductive events for corals and the timing of spawning along the Tuticorin the majority of reef species 5. A wide range of coast and its relationship with the environmental environmental factors may influence the timing of factors were studied in this paper. coral reproduction 6. Coral reefs of the Gulf of Mannar along the Materials and Methods southeastern coast of India are mainly formed around Study sites 21 islands, located between Pamban and Tuticorin. Mainland patch reef (Lat. 8 ° 43´ N, Long. 78 ° 11´ Tuticorin (Lat. 8º 45' N, Long. 78º 10' E) is located at E) - Ten species of Acropora were monitored in this 220 INDIAN J. MAR. SCI., VOL. 39, NO. 2, JUNE 2010

location, Acropora formosa, A. intermedia, was carried out up to April 2007. All the sites are A. microthalma, A. nobilis, A. cytherea, A. shown in the Fig. 1. hyacinthus, A. diversa, A. hemphichi, A. corymbosa, and A. valenciennesi. Monitoring for reproduction

Vaan Island (Lat 8 ° 50´ N, Long. 78 ° 13´ E) - Five The monitoring of reproductive behaviour of the Acropora species were monitored, A. cytherea, Acroporans of Tuticorin region of the Gulf of Mannar A. formosa, A. valenciennesi, A. intermedia and was carried out from January 2006 to March 2008 at A. nobilis. five different locations.

Koswari Island (Lat. 8 ° 52´ N, Long. 78 ° 13´ E) - Monthly samplings were carried out to find out the Because of the relatively low coral cover, only four maturation of coral colonies at all the study sites. Any species A. cytherea, A. formosa, A. valenciennesi and Acropora colony encountered during the survey was A. nobilis, were monitored in this Island since studied. Random samplings were carried out to reduce January 2007. the stress to the same colony. The colonies above 40 cm in diameter were sampled to prevent stressing the ° ° Kariyachalli Island (Lat. 8 57´ N, Long. 78 15´ E) newly growing corals. The reproductive state of - Twelve species of Acropora were monitored, Acropora species was assessed by breaking off a A. cytherea, A. intermedia, A. valenciennesi, branch below the expected sterile zone (5 cm below A. microthalma, A. corymbosa, A. nobilis, A. valida, the tip) 6 and noting the presence or absence of eggs. A. hemphichi, A. hyacinthus, A. stoddarti, A. diversa Unpigmented (immature) are likely to spawn within 1 and A. formosa. to 3 months; visible and pigmented (matured) are Port breakwater area - (Lat. 8 ° 45´ N, Long. 78 ° likely to spawn with in a month and colonies with no 13´ E) – Five species were monitored, A. cytherea, visible eggs (empty) have either just spawned or are A. formosa, A. valenciennesi, A. intermedia and not likely to spawn with in three months 7, 8 (Figs 2 A. nobilis. In the Port breakwater area, monitoring and 3).

Fig. 1—Map showing study sites in Tuticorin coast of the Gulf of Mannar RAJ & EDWARD: REPRODUCTION OF ACOROPORA CORALS 221

Figs 2 & 3—Immature eggs of Acropora nobilis

The timing of spawning was monitored using Results SCUBA at night. Starting from 7 pm dives were made Maturation of gametes with an interval of 30 minutes to investigate the In Acropora species, visible but immature gametes spawning during these suspected nights. Vaan Island were first seen in January during the study years and was concentrated for the spawning observation the percentage of colonies with immature gametes because of its proximity to the shore and relatively increase in the next month and the gametes get good coral cover. Photographs were taken when the coloration and maturity during March and spawn in spawning was observed with underwater digital the same month and the coral colonies do not have camera. Gametes were collected from spawning visible eggs rest of the year in all the study sites. The corals by setting a funnel-shaped bundle-collecting overall average percentage of immature colonies for device (bundle collector) under the water and above A. cytherea in January was between 48-79%; it was the coral colony 9. Bundle collecting devices were set 56-76% in February and matured colonies in March during the suspected spawning season and they were was 36-86%. checked every day. The collected bundles were taken Similarly, the other Acropora species showed 50 to to the lab and the eggs were measured to its nearest 75% of immature colonies in January and an increase margin with Motic Digital Microscope with imaging of 10 to 20% in February, and all the colonies matured Software (Model no. DMB1-223) and photographs in March at all the study sites. The average percentage were taken. of mature colonies in other Acroporans during March in all the study sites throughout the study period was as Physical and chemical parameters follows: A. formosa 47-76%, A. valenciennesi 50-81%, Biophysical parameters such as temperature, A. intermedia 50-81%, A. nobilis 25-82%, salinity, pH, transparency, dissolved oxygen and A. micropthalma 56-83%, A. hemprichi 39-83%, nutrients were analyzed monthly in the water samples A. hyacinthus 33-100% and A. corymbosa 59-65%. The collected from all study locations to study whether details are given in the Tables 1-5. The genus they have any impact on coral reproduction. Montipora is common in all the three islands and lack Temperature was measured with digital thermometer; colouring pattern in gametes; they showed visible salinity was measured using refracto meter; pH was gametes from January to March in the study period. measured with pH meter; transparency was measured Student ‘t’ test analysis showed no significant with secchi disc; dissolved oxygen was measured with difference (P>0.05) between the maturation of the coral Winkler’s method; calcium and magnesium were colonies and sea surface temperature (Table 9). measured titrimetrically; phosphate was measured by 10 the method of Murphy and Riley (1962) ; Nitrates Spawning event and Nitrites were measured spectrophotometrically by Spawning was observed in Acropora cytherea on following Strickland and Parson (1972) 11 . 24 March 2006, 10 days after the full moon. In 2007, 222 INDIAN J. MAR. SCI., VOL. 39, NO. 2, JUNE 2010

Table 1—Average percentage of maturation of Acropora corals in Mainland during 2006-2008

Jan Feb Mar Species M IM E M IM E M IM E Acropora formosa 0 44 56 20 63 17 76 16 8.4 Acropora intermedia 0 46 54 22 67 11 65 23 12 Acropora micropthalma 0 39 28 0 100 0 83 17 0 Acropora nobilis 0 50 50 21 75 5 82 8 10 Acropora cytherea 0 53 47 31 60 9 71 14 14 0 50 50 0 56 11 100 0 0 Acropora diversa 0 67 33 0 83 17 72 17 11 Acropora hemprichii 0 33 33 0 67 0 83 0 17 Acropora corymbosa 0 60 40 18 60 22 65 23 23 Acropora valenciennesi 0 48 52 22 68 9 69 12 19 Table 2—Average percentage of maturation of Acropora corals in Vaan Island during 2006-2008 Jan Feb Mar Species M IM E M IM E M IM E Acropora cytherea 0 79 21 13 76 12 86 5 9 Acropora formosa 0 65 35 24 69 7 72 2 26 Acropora valenciennesi 0 75 25 17 83 0 82 10 8 Acropora intermedia 0 76 24 0 100 0 81 11 8 Acropora nobilis 0 71 29 7 82 34 68 9 23 Table 3—Average percentage of maturation of Acropora corals in Koswari Island during 2007-2008

Jan Feb Mar Species M IM E M IM E M IM E Acropora cytherea 0 73 21 27 67 12 76 10 15 Acropora formosa 0 61 24 30 66 20 64 13 24 Acropora valenciennesi 0 90 10 10 80 10 100 0 0 Acropora nobilis 0 83 13 17 79 9 75 8 17 Table 4—Average percentage of maturation of Acropora corals in Kariyachalli Island during 2006-2008

Jan Feb Mar Species M IM E M IM E M IM E Acropora cytherea 13 69 18 18 67 16 66 24 11 Acropora intermedia 0 57 43 4 79 17 56 44 0 Acropora valenciennesi 6 61 50 15 69 17 53 35 12 Acropora micropthalma 0 67 33 0 67 0 56 11 0 Acropora corymbosa 6 67 28 23 77 17 59 34 7 Acropora nobilis 3 61 39 17 71 12 53 36 11 Acropora valida 0 50 50 0 89 11 50 0 33 Acropora hemprichii 0 33 67 17 67 17 39 28 17 Acropora hyacinthus 17 50 33 0 83 17 33 50 0 Acropora stoddarti 0 100 0 0 89 11 50 0 17 Acropora diversa 0 83 17 0 67 33 28 22 50 Acropora formosa 13 70 16 17 67 16 59 27 13 RAJ & EDWARD: REPRODUCTION OF ACOROPORA CORALS 223

Table 5—Average percentage of maturation of Acropora corals in Harbour breakwater during 2006-2007 Jan Feb Mar Species M IM E M IM E M IM E Acropora cytherea 0 48 52 9 56 35 36 41 24 Acropora formosa 0 31 69 14 48 39 47 10 43 Acropora valenciennesi 0 50 50 17 53 30 25 50 25 Acropora intermedia 0 34 71 0 75 25 50 39 11 Acropora nobilis 0 20 80 6 33 61 25 15 60 Table 6—The level of temperature from January 2006 to December 2006

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Sites (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) Mainland 27.5 29 29 32.5 31.5 30 30.5 30 29.5 28.5 28 27.5 Vaan 27.5 29.5 30 31.5 32 30.5 30.5 30 28.5 29 28.5 26.5 Kariyachalli 27.8 29.5 29 31.5 32 31 30.5 30.5 28.5 29.5 28 27.5 Koswari - - - 31.2 31.5 30.5 30.5 29.5 30 28.5 29 26.8 Harbour 28 29 29 31.2 32 31.5 30.5 29.5 28.5 28.5 28 27 Table 7—The level of temperature from January 2007 to December 2007 Sites Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) (ºC) (ºC)

Mainland 27.5 28 30 31.5 32.9 32.1 30.8 30.1 29.2 27.9 27.4 26.8 Vaan 26.5 27 29.5 31.5 32.7 31.9 30.6 29.9 28.8 27.7 27.3 26.5 Kariyachalli 27.8 28 30.5 31 32.8 31.8 30.5 29.9 29.1 28.3 27.6 26.9 Koswari 27.9 28.2 30.2 31.4 33.2 32.1 30.7 30.1 29.4 28.6 27.9 27.2 Harbour 27.5 28.5 30.5 31.2 32.5 31.6 30.5 29.8 29.2 28.6 28.1 27.6

Table 8—The level of temperature from January 2008 to March Table 9—Student ‘ t’ test analysis between Temperature and Coral 2008 maturity in all the study sites Jan Feb Mar Sites Study sites df t Stat P Value Remarks (ºC) (ºC) (ºC) Mainland 2 0.0634 0.9551 >0.05 Mainland 27.5 30.6 31.4 Vaan 2 0.0965 0.9319 >0.05 Vaan 27.8 30.8 31.5 Koswari 2 0.1903 0.8666 >0.05 Kariyachalli 27.8 30.8 31.7 Kariyachalli 2 0.5083 0.6617 >0.05 Harbour breakwater 2 1.2302 0.3436 >0.05 Koswari 28.3 31.2 32.1 Harbour - - - p<0.05 – significant; p>0.05 - not significant was observed on 28 March, which is 5 days before the to 25 eggs in A. cytherea during 2006. Fecundity rate full moon, and gametes were collected from the was 35 to 40000 egg and sperm bundles per 1 litre of species A. cytherea . In 2008, spawning was observed water in the same species during 2007, and each was on the 8 and 9 March which was 2 days after new having 8 to 15 eggs. Size of each egg was around 24 moon. All the branching corals spawned at the night µm in diameter (Figs. 6 and 7). of 8 th March at 8.50 pm and spawning lasted 15 minutes. On 9 March, spawning was observed only in Physical and chemical parameters A. cytherea at 9.20 pm and it lasted for 10 minutes Sea surface temperatures were between 26.5ºC and (Figs 4 and 5). 33.2ºC throughout the study period with the highest value observed in May 2007 on reefs at Koswari Fecundity Island and the lowest in December 2006 and 2007 at Approximately 30,000 egg and sperm bundles were Vaan Island. It is globally accepted that sea surface collected in one litre of water and each bundle has 20 temperature plays a vital role in coral reproduction 12 . 224 INDIAN J. MAR. SCI., VOL. 39, NO. 2, JUNE 2010

Figs 4 & 5—Spawning of Acropora cytherea

Figs 6 & 7—Spawned gametes of Acropora cytherea

Coral spawning is stimulated by the sudden increase in µg/l. Nitrate content was between 0.23 and 0.68 µg/l water temperature from around 27ºC to 30ºC. and nitrite content was between 0.009 and 0.048 µg/l. Temperature patterns during the study period are shown in the Tables 6-8. Salinity fluctuation was Discussion between 34‰ and 36‰ and pH values between 7.5 Sexual reproduction of Scleractinian corals has and 8.2. Transparency was very low during April to been reviewed by Fadalallah, 1983 13 , Richmond and June every year, with secchi disk readings between 0.5 Hunter, 1990 2, Harrison and Walace, 1990 14 , to 2 m at all the study sites. Transparency was Richmond, 1997 15 . Most coral reproduction studies reasonably high during November to March and it was have been carried out in the Caribbean, the Great between 3.5 to 5 m. Barrier Reef, the Central Pacific and the . The dissolved oxygen level in all the study sites fell Studies in the Asia-Pacific region are restricted to between 3.3 mg/l and 5.8 mg/l. The highest calcium Okinawa (Japan), Taiwan, Philippines, Palau, Papua content was recorded in Vaan Island in December 2006 New Guinea and Singapore. Data from different with 560 mg/l and the lowest in the mainland in regions show different patterns, with considerable February 2007 with 320 mg/l. The amount of variation in mode of reproduction, timing, and magnesium was between 1120 mg/l and 1520 mg/l synchrony among species. throughout the study period in all the study sites. In contrast, very few studies have been carried out Phosphate content was between 1.15 µg/l and 3.59 on coral reproduction in the Indian Ocean 16 . RAJ & EDWARD: REPRODUCTION OF ACOROPORA CORALS 225

Surprisingly, there is no evidence in the timing of The timing of coral spawning can be related to coral reproduction in Southeast Asia, a region that certain environmental factors; it has been suggested contains more than 30% of the world’s reef area and that coral spawning is synchronized by: (i) the annual is home to 600 of the almost 800 scleractinian sea temperature cycle acting as a seasonal cue; (ii) the species 17 . This lack of basic information is worrying lunar phase acting as a fine tuner for a particular as an estimated 88% of Southeast Asia’s reefs are night(s) and (iii) the onset of darkness and tidal threatened by human activities 17 . regimes serving as a forcing function which

Richmond and Hunter, 1990 2 reported that, in determines the actual timing of spawning. In this way equatorial regions where sea surface temperature the release of gametes takes place after nightfall range and tidal amplitude are often small, following the first full moon or new moon subsequent to the maturation of gonads 10,13,14,24,25 . reproductive seasonality and synchrony between species would be reduced. Oliver et al. (1988) 18 It is widely accepted phenomenon that sudden reported a reduction in spawning synchrony in 3 elevation of temperature is the primary and utmost scleractinian species studied at 5 locations along inducer for the coral spawning in most of the reefs. latitudinal gradient ranging from the southern Great Even though temperature fluctuation is not great in Barrier Reef to the northern coast of Papua New the Gulf of Mannar, the sudden increase in the Guinea. Mangubhai and Harrison, 2008 19 viewed that temperature from 27 to d 30 º C happens in March at spawning synchrony in broadcast spawning corals the beginning of the summer. This sudden increase in tends to breakdown with proximity to the equator. In the temperature coincides with coral spawning in the spite of Singapore’s proximity to the equator, Gulf of Mannar. The spawning was observed in Vaan multispecific synchronous coral spawning was Island 10 days after the full moon in 2006, 5 days documented in 2002 occurring after the March full before the full moon in 2007 and 2 nights after new moon 20 . Spawning slicks were observed in March moon in 2008. Student ‘t’ test analysis of temperature 1997 at Ari in the 21 . Baird et al. with coral maturity shows insignificant results but this (2001) 22 observed that 28 of 41 Acropora species small fluctuation in temperature makes an impact on contained mature eggs in the week prior to the full coral spawning. The lunar cycle provides a strong, moon in November 1999. Mangubhai, 2008 16 predictable set of environmental cues for marine documented that the peak spawning period for species. Environment cycles entrain endogenous Acropora species in Kenya is between January and reproductive cycles, synchronizing gamete release April. within a population and ensuring that movement,

In the present study, eggs were seen from January feeding and reproduction occur under favourable 26,27 in each study year in almost all the species of conditions . The other physico-chemical Acropora and mature pigmented gametes were seen in parameters like salinity, pH, transparency, dissolved March and spawning in the same month. All the oxygen and nutrients were well within the limits and monitored Acropora species had mature gametes in did not show any fluctuation during the spawning all study sites during March. This was also supported season. by observations of spawning of Acroporans in the The present study gives baseline information on same month for 3 consecutive years and collection of coral reproduction particularly maturation season and gametes from Acropora cytherea . The timing of the spawning times in Tuticorin coast of the Gulf of reproductive maturity in Gulf of Mannar is supported Mannar. Since coral gametes and larvae can be taken by the findings from Singapore and Maldives which to distant places from the parent reef 28 by the waves are comparatively closer to this area. Guest et al. , and currents, new reef can be created in this worst 2005 23 suggests that a large range in annual sea damaged reef area. After the 2004 Indian Ocean surface temperature is not a pre-requisite for tsunami, people living along Gulf of Mannar coast reproductive seasonality or multi-species spawning realized that coral reefs are important to protect their synchrony. Even though breakdown in the coast from natural disasters and hence they reproductive synchrony has been reported widely, as voluntarily stopped destructive activities, particularly in Singapore reproductive synchrony has been coral mining and thus reduced the disturbances to observed in the Gulf of Mannar also where the substrate for the newly settling coral larvae. Because temperature fluctuation is not very high. of the decrease of human disturbances, and successful 226 INDIAN J. MAR. SCI., VOL. 39, NO. 2, JUNE 2010

reproduction, recruitment and growth there is a 14 Harrison P & Wallace C, Reproduction, dispersal and significant increase in the live coral cover of about recruitment of scleractinian corals, in: Ecosystems of the 29 World, vol. 25, edited by Z. Dubinsky, Coral Reefs , 9.5% in Tuticorin region in the last 36 months . The (Elsevier, Amsterdam) 1990, pp. 133–207. coral reproduction study is in progress in other reef 15 Richmond R H, Reproduction and recruitment in corals: areas in the Gulf of Mannar and also to understand the critical links in the persistence of reefs, in: Life and death of pattern and other factors responsible. coral reefs, edited by C. Birkeland, (Chapman and Hall, New York) 1997, pp. 175–197.

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