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

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1 Indian Journal of Marine Sciences Vol. 39(2), June 2010, pp Observations on the reproduction of Acropora corals along the Tuticorin coast of the Gulf of Mannar, Southeastern India K Diraviya Raj & J K Patterson Edward Suganthi Devadason Marine Research Institute, 44-Beach Road, Tuticorin , Tamil Nadu, India [ diraviyam_raj@yahoo.co.in] 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 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 %, 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 eggs in A. cytherea. Environmental parameters, especially rise in temperature at the end of March was believed to play lead role in coral spawning. [Keywords: Acropora, Spawning, Immature, Mature, Reproduction] Introduction The life cycle of corals includes a free-living planktonic planula phase and a sessile polyp phase, and various asexual and sexual modes of reproduction. Spawning to the process in which corals release sperm and eggs to be fertilized externally 1. Sexual reproduction in corals involves the process of gametogenesis, which may require from a few weeks to over 10 months 2. Coral spawning and reproduction allow corals to inhibit other geographic areas and recover from damage of stressful events. During their larval stage, corals can travel longer distances and can eventually settle on reefs quite far from where were spawned 3. With reef degradation and destruction occurring on a global scale 4, an application of the reproductive data is necessary in the area of reef restoration. Even though sexual reproduction is one of the most important processes for the persistence of reefs, little is known about the factors that regulate reproductive events for the majority of reef species 5. A wide range of environmental factors may influence the timing of coral reproduction 6. Coral reefs of the Gulf of Mannar along the southeastern coast of India are mainly formed around 21 islands, located between Pamban and Tuticorin. Tuticorin (Lat. 8º 45' N, Long. 78º 10' E) is located at the southern end of the Gulf of Mannar Marine National Park. Different reef types such as platform, patch and fringing type are observed in the Gulf of Mannar. The islands have dominantly fringing reefs and also patch reefs around them. Narrow fringing reefs are located mostly at a distance of 50 to 100 m from the islands. On the other hand, patch reefs rise from depths of 2 to 9 m and extend to 1 to 2 km in length with width as much as 50 m. Reef flats are extensive in almost all the reefs in the Gulf of Mannar. Reef areas of the Tuticorin coast in the Gulf of Mannar have been severely damaged due to anthropogenic activities, in particular coral mining, dynamiting and other destructive practices, and hence it is important to have a basic data base on the coral reproduction in this area. In India, the study on coral reproductive biology is new to science and this study is first such effort. Reproductive maturity of the Acropora corals and the timing of spawning along the Tuticorin coast and its relationship with the environmental factors were studied in this paper. Materials and Methods Study sites Mainland patch reef (Lat N, Long E) - Ten species of Acropora were monitored in this

2 220 INDIAN J. MAR. SCI., VOL. 39, NO. 2, JUNE 2010 location, Acropora formosa, A. intermedia, A. microthalma, A. nobilis, A. cytherea, A. hyacinthus, A. diversa, A. hemphichi, A. corymbosa, and A. valenciennesi. Vaan Island (Lat 8 50 N, Long E) - Five Acropora species were monitored, A. cytherea, A. formosa, A. valenciennesi, A. intermedia and A. nobilis. Koswari Island (Lat N, Long E) - Because of the relatively low coral cover, only four species A. cytherea, A. formosa, A. valenciennesi and A. nobilis, were monitored in this Island since January Kariyachalli Island (Lat N, Long E) - Twelve species of Acropora were monitored, A. cytherea, A. intermedia, A. valenciennesi, A. microthalma, A. corymbosa, A. nobilis, A. valida, A. hemphichi, A. hyacinthus, A. stoddarti, A. diversa and A. formosa. Port breakwater area - (Lat N, Long E) Five species were monitored, A. cytherea, A. formosa, A. valenciennesi, A. intermedia and A. nobilis. In the Port breakwater area, monitoring was carried out up to April All the sites are shown in the Fig. 1. Monitoring for reproduction The monitoring of reproductive behaviour of the Acroporans of Tuticorin region of the Gulf of Mannar was carried out from January 2006 to March 2008 at five different locations. Monthly samplings were carried out to find out the maturation of coral colonies at all the study sites. Any Acropora colony encountered during the survey was studied. Random samplings were carried out to reduce the stress to the same colony. The colonies above 40 cm in diameter were sampled to prevent stressing the newly growing corals. The reproductive state of Acropora species was assessed by breaking off a branch below the expected sterile zone (5 cm below the tip) 6 and noting the presence or absence of eggs. Unpigmented (immature) are likely to spawn within 1 to 3 months; visible and pigmented (matured) are likely to spawn with in a month and colonies with no visible eggs (empty) have either just spawned or are not likely to spawn with in three months 7, 8 (Figs 2 and 3). Fig. 1 Map showing study sites in Tuticorin coast of the Gulf of Mannar

3 RAJ & EDWARD: REPRODUCTION OF ACOROPORA CORALS 221 Figs 2 & 3 Immature eggs of Acropora nobilis The timing of spawning was monitored using SCUBA at night. Starting from 7 pm dives were made with an interval of 30 minutes to investigate the spawning during these suspected nights. Vaan Island was concentrated for the spawning observation because of its proximity to the shore and relatively good coral cover. Photographs were taken when the spawning was observed with underwater digital camera. Gametes were collected from spawning corals by setting a funnel-shaped bundle-collecting device (bundle collector) under the water and above the coral colony 9. Bundle collecting devices were set during the suspected spawning season and they were checked every day. The collected bundles were taken to the lab and the eggs were measured to its nearest margin with Motic Digital Microscope with imaging Software (Model no. DMB1-223) and photographs were taken. Physical and chemical parameters Biophysical parameters such as temperature, salinity, ph, transparency, dissolved oxygen and nutrients were analyzed monthly in the water samples collected from all study locations to study whether they have any impact on coral reproduction. Temperature was measured with digital thermometer; salinity was measured using refracto meter; ph was measured with ph meter; transparency was measured with secchi disc; dissolved oxygen was measured with Winkler s method; calcium and magnesium were measured titrimetrically; phosphate was measured by the method of Murphy and Riley (1962) 10 ; Nitrates and Nitrites were measured spectrophotometrically by following Strickland and Parson (1972) 11. Results Maturation of gametes In Acropora species, visible but immature gametes were first seen in January during the study years and the percentage of colonies with immature gametes increase in the next month and the gametes get coloration and maturity during March and spawn in the same month and the coral colonies do not have visible eggs rest of the year in all the study sites. The overall average percentage of immature colonies for A. cytherea in January was between 48-79%; it was 56-76% in February and matured colonies in March was 36-86%. Similarly, the other Acropora species showed 50 to 75% of immature colonies in January and an increase of 10 to 20% in February, and all the colonies matured in March at all the study sites. The average percentage of mature colonies in other Acroporans during March in all the study sites throughout the study period 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 % and A. corymbosa 59-65%. The details are given in the Tables 1-5. The genus Montipora is common in all the three islands and lack colouring pattern in gametes; they showed visible gametes from January to March in the study period. Student t test analysis showed no significant difference (P>0.05) between the maturation of the coral colonies and sea surface temperature (Table 9). Spawning event Spawning was observed in Acropora cytherea on 24 March 2006, 10 days after the full moon. In 2007,

4 222 INDIAN J. MAR. SCI., VOL. 39, NO. 2, JUNE 2010 Table 1 Average percentage of maturation of Acropora corals in Mainland during Acropora formosa Acropora intermedia Acropora micropthalma Acropora nobilis Acropora cytherea Acropora hyacinthus Acropora diversa Acropora hemprichii Acropora corymbosa Acropora valenciennesi Table 2 Average percentage of maturation of Acropora corals in Vaan Island during Acropora cytherea Acropora formosa Acropora valenciennesi Acropora intermedia Acropora nobilis Table 3 Average percentage of maturation of Acropora corals in Koswari Island during Acropora cytherea Acropora formosa Acropora valenciennesi Acropora nobilis Table 4 Average percentage of maturation of Acropora corals in Kariyachalli Island during Acropora cytherea Acropora intermedia Acropora valenciennesi Acropora micropthalma Acropora corymbosa Acropora nobilis Acropora valida Acropora hemprichii Acropora hyacinthus Acropora stoddarti Acropora diversa Acropora formosa

5 RAJ & EDWARD: REPRODUCTION OF ACOROPORA CORALS 223 Table 5 Average percentage of maturation of Acropora corals in Harbour breakwater during Acropora cytherea Acropora formosa Acropora valenciennesi Acropora intermedia Acropora nobilis Sites Jan Table 6 The level of temperature from January 2006 to December 2006 Feb Mar Apr May Mainland Vaan Kariyachalli Koswari Harbour Jun Jul Aug Table 7 The level of temperature from January 2007 to December 2007 Sep Oct Nov Dec Sites Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Mainland Vaan Kariyachalli Koswari Harbour Table 8 The level of temperature from January 2008 to March 2008 Sites Jan Feb Mar Mainland Vaan Kariyachalli Koswari Harbour was observed on 28 March, which is 5 days before the full moon, and gametes were collected from the species A. cytherea. In 2008, spawning was observed on the 8 and 9 March which was 2 days after new moon. All the branching corals spawned at the night of 8 th March at 8.50 pm and spawning lasted 15 minutes. On 9 March, spawning was observed only in A. cytherea at 9.20 pm and it lasted for 10 minutes (Figs 4 and 5). Fecundity Approximately 30,000 egg and sperm bundles were collected in one litre of water and each bundle has 20 Table 9 Student t test analysis between Temperature and Coral maturity in all the study sites Study sites df t Stat P Value Remarks Mainland >0.05 Vaan >0.05 Koswari >0.05 Kariyachalli >0.05 Harbour breakwater >0.05 p<0.05 significant; p> not significant to 25 eggs in A. cytherea during Fecundity rate was 35 to egg and sperm bundles per 1 litre of water in the same species during 2007, and each was having 8 to 15 eggs. Size of each egg was around 24 µm in diameter (Figs. 6 and 7). Physical and chemical parameters Sea surface temperatures were between 26.5ºC and 33.2ºC throughout the study period with the highest value observed in May 2007 on reefs at Koswari Island and the lowest in December 2006 and 2007 at Vaan Island. It is globally accepted that sea surface temperature plays a vital role in coral reproduction 12.

6 224 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 water temperature from around 27ºC to 30ºC. Temperature patterns during the study period are shown in the Tables 6-8. Salinity fluctuation was between 34 and 36 and ph values between 7.5 and 8.2. Transparency was very low during April to June every year, with secchi disk readings between 0.5 to 2 m at all the study sites. Transparency was reasonably high during November to March and it was between 3.5 to 5 m. The dissolved oxygen level in all the study sites fell between 3.3 mg/l and 5.8 mg/l. The highest calcium content was recorded in Vaan Island in December 2006 with 560 mg/l and the lowest in the mainland in February 2007 with 320 mg/l. The amount of magnesium was between 1120 mg/l and 1520 mg/l throughout the study period in all the study sites. Phosphate content was between 1.15 µg/l and 3.59 µg/l. Nitrate content was between 0.23 and 0.68 µg/l and nitrite content was between and µg/l. Discussion Sexual reproduction of Scleractinian corals has been reviewed by Fadalallah, , Richmond and Hunter, , Harrison and Walace, , Richmond, Most coral reproduction studies have been carried out in the Caribbean, the Great Barrier Reef, the Central Pacific and the Red Sea. Studies in the Asia-Pacific region are restricted to Okinawa (Japan), Taiwan, Philippines, Palau, Papua New Guinea and Singapore. Data from different regions show different patterns, with considerable variation in mode of reproduction, timing, and synchrony among species. In contrast, very few studies have been carried out on coral reproduction in the Indian Ocean 16.

7 RAJ & EDWARD: REPRODUCTION OF ACOROPORA CORALS 225 Surprisingly, there is no evidence in the timing of coral reproduction in Southeast Asia, a region that contains more than 30% of the world s reef area and is home to 600 of the almost 800 scleractinian species 17. This lack of basic information is worrying as an estimated 88% of Southeast Asia s reefs are threatened by human activities 17. Richmond and Hunter, reported that, in equatorial regions where sea surface temperature range and tidal amplitude are often small, reproductive seasonality and synchrony between species would be reduced. Oliver et al. (1988) 18 reported a reduction in spawning synchrony in 3 scleractinian species studied at 5 locations along latitudinal gradient ranging from the southern Great Barrier Reef to the northern coast of Papua New Guinea. Mangubhai and Harrison, viewed that spawning synchrony in broadcast spawning corals tends to breakdown with proximity to the equator. In spite of Singapore s proximity to the equator, multispecific synchronous coral spawning was documented in 2002 occurring after the March full moon 20. Spawning slicks were observed in March 1997 at Ari Atoll in the Maldives 21. Baird et al. (2001) 22 observed that 28 of 41 Acropora species contained mature eggs in the week prior to the full moon in November Mangubhai, documented that the peak spawning period for Acropora species in Kenya is between January and April. In the present study, eggs were seen from January in each study year in almost all the species of Acropora and mature pigmented gametes were seen in March and spawning in the same month. All the monitored Acropora species had mature gametes in all study sites during March. This was also supported by observations of spawning of Acroporans in the same month for 3 consecutive years and collection of gametes from Acropora cytherea. The timing of the reproductive maturity in Gulf of Mannar is supported by the findings from Singapore and Maldives which are comparatively closer to this area. Guest et al., suggests that a large range in annual sea surface temperature is not a pre-requisite for reproductive seasonality or multi-species spawning synchrony. Even though breakdown in the reproductive synchrony has been reported widely, as in Singapore reproductive synchrony has been observed in the Gulf of Mannar also where the temperature fluctuation is not very high. The timing of coral spawning can be related to certain environmental factors; it has been suggested that coral spawning is synchronized by: (i) the annual sea temperature cycle acting as a seasonal cue; (ii) the lunar phase acting as a fine tuner for a particular night(s) and (iii) the onset of darkness and tidal regimes serving as a forcing function which determines the actual timing of spawning. In this way the release of gametes takes place after nightfall following the first full moon or new moon subsequent to the maturation of gonads 10,13,14,24,25. It is widely accepted phenomenon that sudden elevation of temperature is the primary and utmost inducer for the coral spawning in most of the reefs. Even though temperature fluctuation is not great in the Gulf of Mannar, the sudden increase in the temperature from 27 to d 30 º C happens in March at the beginning of the summer. This sudden increase in the temperature coincides with coral spawning in the Gulf of Mannar. The spawning was observed in Vaan Island 10 days after the full moon in 2006, 5 days before the full moon in 2007 and 2 nights after new moon in Student t test analysis of temperature with coral maturity shows insignificant results but this small fluctuation in temperature makes an impact on coral spawning. The lunar cycle provides a strong, predictable set of environmental cues for marine species. Environment cycles entrain endogenous reproductive cycles, synchronizing gamete release within a population and ensuring that movement, feeding and reproduction occur under favourable conditions 26,27. The other physico-chemical parameters like salinity, ph, transparency, dissolved oxygen and nutrients were well within the limits and did not show any fluctuation during the spawning season. The present study gives baseline information on coral reproduction particularly maturation season and spawning times in Tuticorin coast of the Gulf of Mannar. Since coral gametes and larvae can be taken to distant places from the parent reef 28 by the waves and currents, new reef can be created in this worst damaged reef area. After the 2004 Indian Ocean tsunami, people living along Gulf of Mannar coast realized that coral reefs are important to protect their coast from natural disasters and hence they voluntarily stopped destructive activities, particularly coral mining and thus reduced the disturbances to substrate for the newly settling coral larvae. Because of the decrease of human disturbances, and successful

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