Galaxea, Journal of Reef Studies (Special Issue): 107-114（2013）

Proc 2nd APCRS

Preliminary observations on the recruitment variability in gratilla (echinodermata: echinoidea) in three selected biogeographic regions in the Philippines

Helen G. BANGI1, *, G. CUARESMA1, Fra-an T. QUIMPO2, Camillia J. BOLLOZOS2, and Hilly A. ROA- QUIAOIT2

1 College of Aquatic Sciences and Applied Technology, Mariano Marcos State University, Currimao, 2903, Ilocos Norte, Philippines 2 McKeough Marine Center, Xavier University, 9000, Cagayan de Oro City, Philippines

* Corresponding author: H.G. Bangi E-mail: [email protected]

Abstract The Tripneustes gratilla is an eco­ the regions, however, the vulnerability of the recruit stage nomically important resource found along reef flats in to the changing environment may differ across biogeo­ many areas in the Philippines. Monthly field monitoring graphic regions. was conducted in three marine biogeographic regions in the Philippines: Northwestern Luzon, Northern Mindanao Keywords Sea urchin, Tripneustes gratilla, Philippines, and Southern Mindanao, to determine and compare the Recruitment variability density and size frequency distribution of T. gratilla benthic recruits (≤40 mm test diameter) from July 2009 to May 2010. Preliminary results showed that the mean density of recruits was significantly higher in the Southern Mindanao Introduction (9.41 individuals/ 100 m2) and Northern Mindanao (5.42 individuals/ 100 m2) compared to Northwestern Luzon The sea urchin Tripneustes gratilla (Linnaeus 1758) is (only 0.28 individuals/ 100 m2). On the other hand, most a high-value resource in many countries including the of the larger-sized urchins (up to 92 mm) were recorded in Philippines. The world production of sea urchins reached the Northwestern Luzon, and adults (＞60 mm) comprised its peak in 1995 with an estimated 120,306 tons fresh up to 66% of the total density. The observed variability in weight (Andrew et al. 2002). However, due to its high the density and size frequency distribution of T. gratilla economic value, many fisheries in the world have become recruits is discussed based on the biophysical profiles of over harvested and depleted. T. gratilla fishery in Bolinao, the three regions. Southern and Northern Mindanao seem Pangasinan in northwestern Philippines is a case study of more favorable for sea urchin recruitment compared to a communal resource exploited without the export market Northwestern Luzon. Our ability to repeatedly induce (Talaue-McManus and Kesner, 1995). Unregulated har­ spawning every month and the prevalence of mature vesting and high market demand for export at the time led stages (up to 100%) of egg samples in the three regions so to a collapse of the multimillion-peso fishery in 1992. far indicate the possible regular supply of larvae in all How­ever, the grow out and restocking efforts of the Uni­ 108 Bangi et al.: Recruitment of Tripneustes gratilla in the Philippines versity of the Philippines Marine Science Institute have enhanced the recovery of the fishery starting in 2000 (Juinio-Meñez et al. 2008a). T. gratilla is also an important resource in the Ilocos and Mindanao regions. Preliminary study on the popu­ lation structure of the species in the Nortwestern Luzon region (Juinio-Meñez et al 2008b; Dela Rosa 2007) showed the abundance of early benthic recruits in Sinait, Ilocos Sur, and in Currimao and Burgos in Ilocos Norte from November 2006 to February 2007. In addition, re­ cruits were also found in Balaoi, Pagudpud, Ilocos Norte and in Northern and Southern Mindanao based on a preliminary study. Anecdotal accounts also indicate a high incidence of early benthic recruits in these areas in the early 1980s to 1990s. A follow up monitoring was done which is important to further understand the pattern and dynamics of recruitment of the species, towards a sus­ tainable strategy for its management. Fig. 1 Map of the Philippines showing the location of the This study was conducted to determine and compare project sites in the South China Sea, Mindanao Sea and Celebes Sea. Filled squares identify the sites the density (individuals/100 m2) and size frequency distri­ bution of T. gratilla recruits (＜40 mm test diameter) in three marine biogeographic regions in the Philippines, from July 2009 to May 2010. T. gratilla from July 2009 to May 2010 (11 sampling time or period), a standard belt transect survey was conducted. At each site, nine (9) 100 m transect lines (or a total of 18 Materials and Methods replicate transects per region) were laid parallel to the shore, approximately 5 m apart. All T. gratilla sea urchins, Study Areas including the benthic recruits (≤40 mm test diameter) The study was conducted as part of an ongoing project found within the belt transects were counted and measured in three marine biogeographic regions in the Philippines, (to the nearest millimeter, mm). Samples of South China Sea (Northwestern Luzon, NL), Mindanao leaves and Sargassum fronds were also randomly collected Sea (Northern Mindanao, NM) and Celebes Sea (Southern within each transect (i.e., about 200 g fronds for every Mindanao, SM) (Figure 1). The specific sites in each re­ 25 m on both sides) to look for early benthic recruits (1.0- gion are located along the reef flats of Ilocos Sur, Ilocos 2.0 mm test diameter). Preserved samples were observed Norte, Northern and Southern Mindanao. Sea surface tem­ under a dissecting microscope, equipped with a micro­ perature data were recorded by installing a thermologger meter. The test diameter of the small T. gratilla were (HOBO water temperature logger, 12-bit resolution and measured to the nearest micrometer (µm). 0.2℃ accuracy precision sensor) in each region. Diffusion rate (DR, in gh−1) which represents the average water Data Analysis movement in an area was determined based on the “clod The mean density (number of individuals per 100 m2) card method” of Doty (1970). per region was computed based on eighteen (18) 100 m2 replicate belt transects. This also included densities of the Sampling early benthic recruits observed under the microscope. To determine changes in densities and size structure of Analysis of variance (ANOVA) was conducted to deter­ Bangi et al.: Recruitment of Tripneustes gratilla in the Philippines 109 mine significant differences across regions and sampling months, followed by Tukey’s Honestly Significant Dif­ ferences (Tukey’s HSD) range test (p＜0.05). The per­ centage frequencies for T. gratilla juvenile recruits were analyzed and compared with other size categories (pre- adults and adults) with respect to regions and sampling period. Prior to ANOVA, percent frequency data were arc- ＜ sine transformed, followed by Tukey’s HSD test (p 0.05). Fig. 2 Overall average density of T. gratilla recruits (＜40 To compare the degree of variability in mean sea surface mm, in solid bar (■) and non-recruits) in three biogeographic temperature, the coefficient of variation (CV) were deter­ regions over eleven months sampling period. Values for Norwestern Luzon smaller than solid bar symbol mined for each region. Correlation analysis was also done to determine the possible relationship between sea surface temperature readings and the density of recruits in the three regions. CV＝0.058; range: 20.84-32.30℃) compared to Northern Mindanao (CV＝0.027; range: 25.91-31.20℃, mainly in Murcielagos) and Southern Mindanao (CV＝0.0197; Results range: 28.10-31.61℃, mainly in Sta Cruz). Moreover, the maximum temperature values recorded in Northwestern Density Luzon sites were higher compared to Northern and Significant spatial variations were observed in the mean Southern Mindanao. Correlation analysis on sea surface density of T. gratilla recruits (＜40 mm test diameter) in temperature and the density of T. gratilla recruits revealed three biogeographic regions in the Philippines. Overall, highly significant negative correlation, though the rela­ very low density (individuals/100 m2) of recruits was tionship is relatively weak. In addition to sea surface observed in Northwestern Luzon from July 2009 to May temperature, water movement (expressed as diffusion 2010, compared to Northern and Southern Mindanao rate, in ghr−1) was very high in Northwestern Luzon sites regions. There was only an average of 0.28±0.74 re­ (up to 527 ghr−1 in Pagudpud and 346 ghr−1 in Sinait, cruits/100 m2 recorded in the Northwestern Luzon region, Figure 4). and this was significantly lowerp ( ＜0.05) compared to the overall average densities found in Northern Mindanao Size Frequency Distribution (5.42±2.83) and Southern Mindanao (9.41±1.33) re­ The size frequency distributions (SFD) of T. gratilla in gions (Figure 2). No significant difference was found in the three regions are shown in Figure 5. The SFD during the overall average density of recruits between Northern the 11-month sampling period generally showed a uni­ Mindanao and Southern Mindanao regions (p＞0.5). modal distribution throughout most months. While significant variations were observed in the average The relative percentage of recruits (＜40 mm TD) to densities of recruits across three regions, in general, no pre-adult (40-60 mm TD) and adult T. gratilla (＞60 mm significant variation was found across sampling months TD) varied with respect to the sampling regions. The (p＞0.05). percentage of recruits in Northwestern Luzon region was Based on sea surface temperature time series data, the significantly lower (7.42%) compared to pre-adult (26.28 daily change in temperature in Northwestern Luzon sites %) and adult (66.31%) urchins during most of the sam­ is more variable compared to the records in Northern and pling months. On the other hand, the percentage of recruits Southern Mindanao regions (Figure 3a-3d). The variability in Northern and Southern Mindanao regions were sig­ in mean sea surface temperature was higher in North­ nificantly higher (24.17% and 48.34%, respectively) com­ western Luzon sites (Coefficient of Variation or CV＝ pared to the percentage of adults (18.12% and 3.86%, 0.062; range: 22.78-35.82℃ in Sinait and in Pagudpud: respectively). While significant variations were observed 110 Bangi et al.: Recruitment of Tripneustes gratilla in the Philippines

Fig. 3a Time series sea surface temperature profile in Sinait (NL) from February 23, 2010 to March 26, 2010

Fig. 3b Time series sea surface temperature profile in Pagudpud (NL) from February 24, 2010 to March 25, 2010

Fig. 3c Time series sea surface temperature profile in Murceilagos (NM) from March 19, 2010 to April 18, 2010

Fig. 3d Time series sea surface temperature profile in Sta Cruz (SM) from March 9, 2010 to April 15, 2010 Bangi et al.: Recruitment of Tripneustes gratilla in the Philippines 111

and the density of T. gratilla recruits revealed highly sig­ nificant negative correlation, though the relationship is relatively weak. According to Lawrence and Agatsuma (2001), T. gratilla can tolerate lower temperature (as low as 10℃) more than higher temperature. These results, together with the observed higher coefficient of variation in sea surface temperature in Northwestern Luzon sites, may possibly and partly explain the lower densities of recruits in this region compared to the two Mindanao

Fig. 4 Mean diffusion (gh−1) readings in two study sites in regions. In addition, though water movement was not NL from November, 2009 to May 2010 monitored regularly in Mindanao regions due to logistical concerns, actual observation showed relatively calmer water in these regions compared to Northwestern Luzon. in the size frequency distribution of T. gratilla recruits NL region is more exposed to strong wave action and relative to other size categories across sampling regions, higher frequency of storms compared to Mindanao re­ no significant variation was observed across sampling gions. These possibly indicate a more favorable condition months. Although there was significant difference in the for sea urchin recruitment in Mindanao region compared percentage of adults across regions, the results of the to Northwestern Luzon. The drastic periodic disturbance monitoring done by the other project component on re­ (strong wave action and the recurring typhoons) in productive stages based on egg samples (Figure 6) in five Northwestern Luzon may also be a source of juvenile/ specific sites indicate a very high (up to 100%) prevalence­ recruits mortality in the area. A continuous and long term of mature stages in all the sites throughout most of the monitoring of sea surface temperature and other related sampling months. parameters, however, will give a better picture of the variability of these parameters across regions and time. Aside from physical processes, other processes such as Discussion differential recruitment success may affect population structure and density. This is manifested in the variability Significant variations were observed in the density and in the magnitude and timing of the occurrence of recruits size frequency distribution of T. gratilla across three at different regions, although the difference was not sig­ regions in the Philippines. In general, mean density of nificant. recruits in Northwestern Luzon was significantly lower The habitats in the sites monitored in Northwestern compared to Northern and Southern Mindanao, across Luzon region are very similar, likewise those in northern eleven sampling months. This preliminary observation of and Southern Mindanao region. The two sites in NL are variability can be explained initially by the biophysical seagrass beds dominated by Thalassia hemprichii and differences of the three regions, though this may be due to Sargassum beds with patches of coral heads, the interplay of physical and biological factors. Based on rocks covered with Sargassum and rubbles. The sites in sea surface temperature time (SST) series data, the daily the two Mindanao regions are dominated by seagrass change in temperature in Northwestern Luzon is more Thalassia hemprichii. These seagrass and are variable compared to the records in Northern and Southern usually found abundant in the study sites, serving as food Mindanao regions. This confirms a previous result (David for T. gratilla, hence the availability of food in the sites is and Borja, in prep.) on SST in 1985 to 2006. Moreover, possibly out of the question to affect reproduction and the maximum temperature values recorded in Northwestern recruitment of the species. Luzon were higher compared to Northern and Southern Recruitment is also dependent on the availability of Mindanao. Correlation analysis on sea surface temperature larval supply for settlement and metamorphosis, which 112 Bangi et al.: Recruitment of Tripneustes gratilla in the Philippines

Fig. 5 Overall size frequency distribution of T. gratilla (≤10 mm to ≤100 mm) in three biogeographic regions over eleven months sampling period (July 2009 to May 2010). Bangi et al.: Recruitment of Tripneustes gratilla in the Philippines 113

Fig. 6 Percentage frequency of egg stages overlaid on to gonadosomatic index (GSI) data in specific sites in the three regions (Murcielagos Bay and Mantigue Is.in Northern Mindanao, Sta Cruz in Southern Mindanao, and Pagudpud and Sinait in Northwestern Luzon) over a 6 to 9-month sampling period.

largely depend on the reproductive output of the species Menez et al. 2008a). Gonad index values were generally and the synchronous spawning of both sexes. Based on consistent for male and female , indicating syn­ initial results from the project (data not shown here), chronous spawning by both sexes. These results indicate female and male T. gratilla adults have been induced to the possible regular supply of larvae in all the regions, spawn regularly in all the sites. Moreover, gonad samples however, the vulnerability of the recruit stage to the with mature eggs (up to 100%) were always available chang­ing environment may differ across biogeographic during most of the sampling months. These data confirm regions. the very rapid gametogenic cycle in this species (Juinio- The continuation of the monitoring of the population 114 Bangi et al.: Recruitment of Tripneustes gratilla in the Philippines structure of T. gratilla and the conduct of other studies EP, Barnes DKA, Botsford LW, Bradbury A, Campbell such as reproductive seasonality and the hydrographic A, Dixon JD, Einarson S, Gerring P, Hebert K, Hunter M, patterns (to determine larval dispersal mechanisms) is Hur SB, Johnson CR, Juinio-Meñez MA, Kalvass P, Miller important to better understand this preliminary obser­ RJ, Moreno CA, Palleiro JS, Rivas D, Robinson SML, Schroeter SC, Woodby RS, Xiaoqi Z (2002) Status and vations on the variability of recruitment of T.gratilla in management of world sea urchin fisheries. Oceanogr Mar the three regions. Biol Annu Rev 40: 343-425 Dela Rosa RJ (2007) Spatio-temporal variations in density and size frequency distribution of the sea urchin Tripneustes Acknowledgements gratila (Linn. 1758; Echinodermata Echinoidea) in three sites of Ilocos. Undergraduate Thesis, Mariano Marcos This study was conducted as part of an ongoing re­ State University, The Philippines search project on “Invertebrate Fisheries Populations as David L and Borja R (in prep) Constantly changing climate: SST Response Indicators for Climate Change” under a national signals in the Philippines. Marine Science Institute, Uni­ program: “Integrated Coastal Enhancement: Coastal Re­ versity of the Philippines search, Evaluation­ and Adaptive Management (ICE Doty SM (1970) Movement of water movement in reference to CREAM), funded by the Philippine Council for Aquatic benthic algal growth. Botany Department, University of and Marine Resources Development - Department of De­ Hawaii, Honolulu, Hawaii, pp 11-10 partment of Science and Technology (PCAMRD-DOST). Juinio-Meñez MA, Bangi HG, Malay MC, Pastor D (2008a) Enhancing the Recovery of Depleted Tripneustes gratilla Monitoring of sea urchins in the Northwestern Luzon Stocks Through Grow-out Culture and Restocking. Rev region is part of the project’s activities in collaboration Fish Sci 16(1-3): 35-43 with the Mariano Marcos State University based in Cur­ Juinio-Meñez MAJ, Pastor D, Bangi HGP (2008b) Indications rimao, Ilocos Norte. Monitoring in the two Mindanao of recruitment enhancement in the sea urchin Tripneustes sites are done primarily by the Research Staff based at the gratilla due to stock restoration efforts. Proc 11th Int Coral Xavier University, Cagayan de Oro City. The DOST- Reef Symp: 1017-1021 PCAMRD provided travel support for HGPB to participate Lawrence JM, Agatsuma Y (2001) The ecology of Tripneustes. nd at the 2 APCRS in Phuket, Thailand on June 19-24, In: Lawrence JM (ed) Edible Sea urchins: Biology and 2010. We are grateful to our enumerators, thesis students Ecology, Elsevier, pp 395-413 and student assistants for their invaluable support in the Talaue-McManus L, Kesner KP (1995) Valuation of a Philippine field and laboratory collection of data. Ms. Gretchell Lou municipal sea urchin fishery and implications of its Gomez provided assistance for financial logistics. collapse. In: Juinio-Meñez MAR, Newkrik GF (eds.) Phil­ ippine coastal resources under stress, Selected papers from the Annual Common Property Conference, Manila, June - - References 16 19, 1993, pp 229 239

Ⓒ Japanese Society Andrew NL, Agatsuma Y, Ballesteros E, Bazhin AG, Creaser