Seasonal Occurrence and Aggregation Behavior of the Sea Urchin Astropyga Pulvinata (Echinodermata: Echinoidea) in Bahı´A Culebra, Costa Rica1

Home , Astropyga, Astropyga radiata, Diadematidae, Diadema mexicanum, Diadema setosum

Seasonal Occurrence and Aggregation Behavior of the Sea Urchin Astropyga pulvinata (Echinodermata: Echinoidea) in Bahı´a Culebra, Costa Rica1

Juan Jose´Alvarado2

Abstract: Between October 2003 and July 2005, aggregation behavior of the sea urchin Astropyga pulvinta Lamarck was studied in Bahıá Culebra, Costa Rica. This sea urchin forms aggregations during part of the year and then disappears. I quantified the number of individuals present in a defined area each month, their aggregation behavior between day and night, and their size. Also, temperature and nutrient concentrations of the water were sampled. There were signif- icantly more individuals in aggregations during the colder, upwelling season (December to April). Aggregations consisted of adult individuals that exploit food during the upwelling season. Moreover, these aggregations were used as a refuge by several fish species of high commercial value for the aquarium trade. These sea urchin populations could suffer as extraction of ornamental fishes and urchins increases. Their abundance and behavior should continue to be moni- tored as an indication of the ecological health of the community.

Diadematid sea urchins are among the reef areas due to their substantial effects on most important and familiar inhabitants of the biomass, structure, and distribution of tropical and subtropical waters (Hyman seaweeds, as well as on coral composition 1955). Their ability to occupy different and reef geomorphology because they are niches is an important factor in their success; bioeroders (see review by Birkeland 1989). they live on coral reefs, mangrove roots, sea In the eastern tropical Pacific there are five grasses, and sand flats. Moreover, their suc- diadematid species in four genera: Astropyga, cess is linked to their generalist diet and their Centrostephanus, Echinothrix, and Diadema. efficiency in use of the resources available. The last genus has received more attention They are found in caves, overhangs, and in the eastern Pacific due to the important crevices that provide protection against pred- role of Diadema mexicanum as a reef bio- ators, and they are more abundant in zones eroder and controller of seaweed populations protected from strong waves. For that reason, (Glynn 1988, Guzmań 1988, Fischer 1990, if wave stress increases, or if predators or Guzmań and Corte´s 1992, 2007, Herrera- competitors are present, diadematids tend to Escalante et al. 2005). Also, its reproductive aggregate. They play an important role on cycle and population structure (Lessios 1981, Espino-Barr et al. 1996) have been studied, as well as its phylogeographic relationships 1 Support was provided by Vicerrectorıá de Investiga- (Lessios et al. 2001). With respect to Centro- cioń of the Universidad de Costa Rica, for partial finan- stephanus coronatus, its bioerosional impact cial support through the projects of Jorge Corte´s 808- (Toro-Farmer et al. 2004), role in controlling 96-601 and 808-98-013 and Ecodesarrollo Papagayo. algae (Vance 1979), and reproductive cycle Manuscript accepted 14 December 2007. 2 Centro de Investigacioń en Ciencias del Mar y (Kennedy and Pearse 1975) have been stud- Limnologıá (CIMAR), Universidad de Costa Rica ied. But there are very few papers on Echino- (UCR), 2060 San Pedro, San Jose´, Costa Rica (e-mail: thrix and Astropyga in the eastern Pacific. [email protected]). Members of the genus Astropyga are among the most conspicuous diadematids, Pacific Science (2008), vol. 62, no. 4:579–592 with a series of iridescent blue spots on the : 2008 by University of Hawai‘i Press test, thin spines, and a large, flexible, and All rights reserved very low test (Mortensen 1940, Caso 1978).

579 580 PACIFIC SCIENCE . October 2008

Astropyga is found in tropical and subtropical de Afuera Island, Peru´, they formed numer- waters of the Caribbean, Indo-Pacific, and ous aggregations on rocky reef between 0 eastern Pacific and includes three species and 5 m deep in June 1999 (Hooker et al. (Mortensen 1940): A. magnifyca, A. radiata, 2005). and A. pulvinata. Astropyga pulvinata Lamarck The objective of this work is to describe has been reported from the Gulf of Cali- basic ecological characteristics of Astropyga fornia (Solı´s-Marıń et al. 2005), El Salvador pulvinata in Bahıá Culebra, on the northern (Barraza and Hasbuń 2005), Panama´ (Lessios Pacific coast of Costa Rica. Abundance, den- 2005), Colombia (Neira and Cantera 2005), sity, degree of aggregation, and population the Gala´pagos Islands (Hickman 1998), and structure are described as well as their rela- Lobos de Afuera Island in Peru´ (Hooker tion to several physicochemical parameters, et al. 2005). It occurs on sand, rock, or muddy with the goal of determining the spatial and substrates (Clark 1940, Caso 1978, Hickman temporal extent of aggregations and which 1998) between 2 and 95 m deep (Clark 1948, parameters might control them. Hickman 1998; C. Fernańdez, pers. comm.). It possesses a flat test with triangular white materials and methods areas on the interambulacral zones (Morten- sen 1940) and a maximum test diameter of The study took place between October 2003 120 mm (Brusca 1980). This species eats any and July 2005, at Punta Flor (10 370 26.8000 kind of bottom material with foraminifera N, 85 40 0 45.4 00 W ) (Figure 1) in the inner and small gastropods (Mortensen 1940, De part of Bahıá Culebra on the north Pacific Ridder and Lawrence 1982). In several sec- coast of Costa Rica. This bay is subjected to tions of the American coast, large aggrega- a seasonal upwelling of cool, rich waters be- tions of this sea urchin have been observed, tween December and April (Brenes et al. generally during the upwelling season, but 1990, Jimeńez 2001). It consists of a series of they later disappear (Hickman 1998, Hooker inlets, beaches, sea cliffs, and estuaries with et al. 2005, Lessios 2005). economically important marine resources Diadematid aggregations have been ob- ( Jimeńez 2001). It is a zone rich in coral served in many places around the world, like reefs, with approximately 16 species of reef- the Great Barrier Reef of Australia, in Japan, building corals, and live coral cover of 44% Suez, in the Caribbean, and in the eastern ( Jimeńez 2001). Punta Flor is located on the Pacific (see references in Pearse and Arch inner part of the bay, in the north section. It [1969]). In Huatulco Bay, on the Pacific coast is a zone surrounded by sea cliffs with scarce of Mexico, aggregations of Diadema mexica- vegetation, a narrow intertidal zone, and a sea num composed of hundreds of individuals bottom composed mainly of coarse and me- caused intense grazing on a dead reef of Pocil- dium sand (C. Fernańdez, unpubl. data). lopora (Glynn and Leyte-Morales 1997). Ag- gregations of have been Astropyga pulvinata Biological Variables observed in several localities in the eastern Pacific: in the Gala´pagos Islands (Albany Is- Astropyga pulvinata is a common sea urchin in land) aggregations of two to @300 individuals Bahıá Culebra that in some periods of the in depths around 12 m appear in February year forms aggregations (two or more indi- and disappear in November (Hickman 1998). viduals close together, touching at least by Aggregations have been observed sporadically their spines) (Figure 2). With the goal of un- during some times of the year on Cocos Is- derstanding this behavior, the dynamics of land, and then they disappear suddenly (N. the aggregations were studied between Octo- Gersinich, pers. comm.). In Panama´, during ber 2003 and July 2005 in Punta Flor (Figure the upwelling season, they can be found in 1). The monthly density of the sea urchin great concentrations in the Gulf of Panama´ and the aggregation behavior between day (Changame Island), over sand at approxi- and night were determined by measuring the mately 10 m depth (Lessios 2005). At Lobos distance between individuals. To determine Seasonal Occurrence of Astropyga pulvinata in Costa Rica . Alvarado 581

Figure 1. Punta Flor location in Bahı´a Culebra, sites where Astropyga pulvinata aggregations occur, and nutrient sampling stations inside the bay. abundance, all individuals of the sea urchin tions and the number of sea urchins per ag- were counted monthly in an area of 3,125 gregation. The sampling always took place m2 (125 m long by 25 m wide). The area was between 0800 and 1000 hours. Between No- covered in a zigzag manner from around 2 m vember 2003 and February 2004 night dives depth down to 8–10 m (approximately 25 m were done, between 1830 and 2000 hours, to from the coastline), counting all the aggrega- observe the nocturnal aggregation behavior. 582 PACIFIC SCIENCE . October 2008

Figure 2. Astropyga pulvinata adult aggregation at Punta Flor, Bahı´a Culebra.

The diameter of the test was measured, be- done to determine if there were differences tween November 2003 and September 2004 between: (a) the total number of individuals with a caliper, to define population struc- per month (or density) and the season of the ture over time. Ten individuals were mea- year (upwelling and nonupwelling); (b) the sured per aggregation, so the total number distance between individuals and the time of measured depended on the number of aggre- day; (c) the number of aggregations and the gations during the sampling dive. This proce- time of day; (d) the total number of individu- dure followed the same zigzag pattern, always als per sampling and the time of day; and (e) measuring and counting the urchins in the the average of individuals per aggregation same direction to avoid counting the same in- and the time of day. dividuals twice. Finally, between January and February Physicochemical Variables 2004, the distance between individuals was measured with a metric tape from the border As part of a Centro de Investigacioń en Cien- of the test of the urchin to the nearest neigh- cias del Mar y Limnologıá (CIMAR) moni- bor test, during the day and night, to deter- toring program, seawater temperature was mine if there is a higher or lower degree of recorded every 30 min with a data logger aggregation depending on the time of the (StowAway) located at 6 m depth on the Playa day. We counted a minimum of 50 individu- Blanca reef (Figure 1). The concentration of 3 als per dive. The results are presented as phosphate (PO4 ) at three stations in the bay averages G the standard deviation. (E1, E2, E3) (Figure 1) was determined as a Nonparametric Kruskal-Wallis tests were proxy of the productivity of the environment. Seasonal Occurrence of Astropyga pulvinata in Costa Rica . Alvarado 583

Figure 3. Total individuals of Astropyga pulvinata observed per month (columns), monthly average seawater temperature (C, open triangles), and average phosphorus concentration (mM, open diamonds) at Punta Flor, Bahı´a Culebra. No phosphorus determinations were available for April, June, and July 2005. The upwelling season is indicated by gray shading.

Every month at each station, 1 liter of surface rus concentration was 0.23 G 0.15 mM, with water was sampled and later analyzed follow- a maximum value of 0.56 mM in March 2005 ing the procedures of Strickland and Parsons and a minimum of 0.05 mM in August 2004. (1972) using a spectrophotometer (Shimadzu Phosphate followed a pattern opposite to UV-160A). that of temperature, with high values during Linear regressions between monthly aver- the dry season (upwelling) (Figure 3). age temperature and nutrient concentrations, and total numbers of individuals per month Biological Variables were done. All the data were transformed with the function log10ðx þ 1Þ and analyzed Astropyga pulvinata was more abundant dur- with the programs Systat 8.0 (Systat Software ing the upwelling season and almost absent 1998) and JMPin 4.0 (SAS Institute 2001). in the nonupwelling season (Figure 3). An average of 679 G 356 individuals per month was calculated for the upwelling season and results 159 G 226 individuals per month for the nonupwelling season. It was most abundant in Physicochemical Variables January 2004 (1,203 individuals) and absent During the study period, the average sea tem- in June, August, and September 2004 (Fig- perature was 27.8 G 1.57C, being maximal ure 3). A significant difference was detected in September 2004 (29.8C) and minimal in among seasons between the numbers of indi- March 2004 (24.1C), corresponding with viduals (dry versus rainy season) (KW ¼ 10.0, the rainy and the dry (upwelling) season, re- P < .01, n ¼ 22). No relationship was de- spectively (Figure 3). The average phospho- tected between the concentrations of phos- Figure 4. (A) Density (individuals per square meter), (B) number of aggregations, and (C) average and standard deviation of individuals per aggregation of Astropyga pulvinata at Punta Flor, Bahıá Culebra, between October 2003 and October 2005. Figure 5. Comparison of aggregations of Astropyga pulvinata at Punta Flor, Bahıá Culebra, between day and night from November 2003 to February 2004. (A) Total individuals, (B) number of aggregations, and (C) average number of indviduals per aggregation. 586 PACIFIC SCIENCE . October 2008

Figure 6. Average distance (centimeters) and standard deviation between individuals of Astropyga pulvinata in day and night aggregations at Punta Flor, Bahıá Culebra, January and February 2004. phate and the quantity of individuals per one aggregation, and in March 2005 there month, but there was a significant negative were nine aggregations with a total of 559 in- relationship with temperature (R2 ¼ 0.21, dividuals. January 2004, with 24 individuals P < .05). per aggregation, was the month with the The average density was 0.13 G 0.12 in- highest number of individuals (1,203). dividuals per square meter, 0.2 G 0.1 indi- There was no statistical difference between viduals per square meter for the upwelling the average number of individuals during season, and 0.1 G 0.1 individuals per square the day ð610 G 482Þ and during the night meter for the nonupwelling season, with two ð457 G 460ÞðP ¼ :56Þ. There were also no maximal values of 0.38 and 0.37 individuals statistical differences between average num- per square meter for January 2004 and April bers of aggregations during the day 2005, respectively (Figure 4A). The highest ð29:0 G 20Þ and at night ð12:5 G 3:9Þ, or be- numbers of aggregations between 0800 and tween average number of individuals per ag- 1000 hours were observed in January, Feb- gregation in the night ð38:6 G 43:0Þ and in ruary, and April 2004 with 94, 91, and 68 the day ð20:2 G 6:8Þ,(P ¼ :24, P ¼ 0.73, re- aggregations per month, respectively (Figure spectively) (Figure 5). Also, no significant dif- 4B), and an average of 21.6 G 29.3 aggre- ference was found in the distance between gations per month, 40.8 G 34 aggregations individuals in the day (5.9 G 3.1 cm) and the per month for the upwelling season, and night (5.7 G 2.5 cm) (KW ¼ 9,045, P ¼ .08, 5.6 G 9.1 aggregations per month for the n ¼ 261) (Figure 6). nonupwelling season. On average each aggre- Most individuals had a test diameter be- gation had 26.9 G 24.5 individuals. June 2005 tween 70 and 120 mm (101.3 G 3.6 mm) (a nonupwelling month) was the month with (Figure 7). The predominant size was be- the highest number of individuals per aggre- tween 90 and 100 mm, which corresponds to gation (75), followed by March 2005 (69.7) adult size. The @70 mm size corresponds to (Figure 4C). In June 2005 there was only large juveniles, and they had a different color Figure 7. Monthly size (diameter of the test in millimeters) frequency (%) distribution of Astropyga pulvinata at Punta Flor, Bahıá Culebra, between November 2003 and September 2004. For June, August, and September 2004 no individuals were recorded in the area. 588 PACIFIC SCIENCE . October 2008 pattern than the adults. The sizes reported actions (protection when abundant and food herein are within the range reported for the optimization). The aggregates are made up region (15–117 mm) (Clark 1923, 1940, only of adult individuals, which have better 1948, Caso 1961, 1978, Lessios 1990). Clark protection due to their longer spines. Mean- (1948) pointed out, based on a series of col- while, the juveniles protect themselves in lections from the eastern Pacific, that juve- caves or crevices on the rocky or reef areas. niles are between 17 and 35 mm and the During the upwelling season there is adults range between 100 and 117 mm. higher food availability, which is probably the reason the sea urchins come into shallow discussion waters to feed. At that time of year, the thermocline is shallower (between 15 and 20 m) Although aggregations of sea urchins could with a higher zooplankton abundance (Bed- be associated with reproductive activities, in narski and Morales-Ramı´rez 2004). The sea the majority of cases these aggregations ap- urchins may follow the change of the ther- pear to be in response to local environmental mocline position and move to shallow water factors or involved in social interactions to feed, descending when the thermocline (Reese 1966). Three hypotheses have been sinks at the end of the upwelling. Maurer proposed to explain the benefits of these et al. (1980) reported individuals of this spe- aggregations: (1) food optimization, (2) resis- cies on the outer part of the Gulf of Nicoya, tance to predator attack, and (3) improvement in Costa Rica, at 35 m depth. That depth cor- of fertilization success at spawning (see refer- responded with the thermocline zone, where ences in Campbell et al. [2001]). In the case the temperature was close to 20C and the 3 of tropical diadematids these aggregations PO4 concentration was 2 mM (Epifanio et al. represent social activities and do not seem to 1980). In Acapulco Bay (Pacific coast of Mex- be simple responses to environmental limita- ico), many aggregations of 5 to 30 individuals tions (Pearse and Arch 1969). on rocky substrate were associated with the Pearse and Arch (1969) studied the ag- thermocline between 20 and 27 m depth gregation behavior of Diadema setosum in (pers. obs., November 2005). This indicated Bougainville, Papua New Guinea, and deter- that the adult behavior of Astropyga pulvinata mined that they are related to protection, in- is influenced by the behavior of the thermo- stead of reproduction. They suggested that cline related to the disposition of food asso- when urchins are too abundant to find shelter ciated with it. A similar example of urchin among rocks, individuals form aggregations aggregations to exploit food resources was for protection against predators. Moreover, observed in Japan, where Astropyga radiata when a few individuals within an aggregation aggregations reduced an eelgrass (Zostera are disturbed, they interact with others, and maritima) patch (Bak and Nojima 1980), indi- the whole aggregation moves away. cating migration to a food supply. Astropyga pulvinata in Bahıá Culebra may There is a possibility that these aggrega- be aggregating for protection against preda- tions have a role in reproduction. Urchins tors because they presented behavior similar could, for example, enhance fertilization by to that described by Pearse and Arch (1969). being aggregated during spawning. However, However, attacks on sea urchins were not during the study spawning was not ob- observed, and broken tests were found only served. Bauer (1976) found that Diadema antil- rarely. Also, aggregations appear during the larum in Florida aggregated during spawning upwelling season, when there is no evidence months when sea temperatures are low, of an increase of predators. Because Astropyga which worked as a triggering signal. In my spp. are detritivores (Mortensen 1940, De study the focus was not on reproduction, but Ridder and Lawrence 1982), they may be ex- it should be considered in future research. ploiting the food resources produced during Moreover, from size data (Figure 7) the ob- the upwelling season. The aggregations are served phenomenon is not the result of local probably due to a combination of both inter- recruitment of recently metamorphosed sea Seasonal Occurrence of Astropyga pulvinata in Costa Rica . Alvarado 589

TABLE 1 Culebra act as a refuge too. This area of the Organisms Associated with Astropyga pulvinata at Punta country is subjected to much fish extraction Flor, Bahıá Culebra for aquariums (Corte´s 1996–1997, Ibarra 1996), so the urchins could have a high con- Group Family Species servation value for several fish species in the region. Crustaceans Inachidae Stenorhynchus debilis In the past few years, the local people of Fishes Serranidae Alpheste multiguttatus Dermatolepis dermatolepis Bahıá Culebra have seen a reduction of the Grammistidae Rypticus bicolor populations of Astropyga pulvinata, which is Apogonidae Apogon dovii being extracted for the aquarium trade. Con- Apogon pacifici sequently, it important to continue monitor- Haemulidae Not identified Lutjanidae Lutjanus guttatus ing these populations and the impact of their Chaetodontidae Chaetodon humeralis disappearance on other species. Pomacanthidae Pomacanthus zonipectus Labridae Halichoeres dispilus acknowledgments I am grateful to Cindy Fernańdez, Davis urchins but rather the immigration of adult in- Morera, Jaime Nivia, Eddy Gomez, Eva dividuals from elsewhere. Salas, Mario Espinoza, Bernadette Bezy, Ele- The diadematids have been recognized as azar Ruiz, The Instituto Costarricense de Tu- refuges for several species of fishes, favoring rismo, and Ecodesarrollo Papagayo for their the development of juvenile stages and in collaboration. The manuscript was enriched some cases adults and serving as biogenic by comments from Jorge Corte´s, John Law- structures that provide protection (Randall rence, John Pearse, and two anonymous re- et al. 1964, Teytaud 1971, Hartney and viewers. Grorud 2002, Kolm and Berglund 2003). In my study, 10 species of fishes and one crab Literature Cited species (Stenorhynchus debilis) were observed associated with the Astropyga aggregations Bak, H., and P. Nojima. 1980. Immigration (Table 1). The fishes that were found most of tropical sea urchin, Astropyga radiata often were adults of Rypticus bicolor, which (Leske) in a temperate eelgrass, Zostera dig under the urchin spines, and two species marina L., patch: Its feeding habit and of Apogon. The first species was observed grazing effect on the patch. Amakusa Mar. close to the sand, under the spines of the ur- Biol. Lab. 5:153–169. chin, and the apogonids were observed be- Barraza, J. E., and C. R. Hasbuń. 2005. Los tween the spines in high numbers. Apogon equinodermos (Echinodermata) de El Sal- is commonly associated with diadematid ag- vador. Rev. Biol. Trop. 53 (Suppl. 3): 139– gregations (Kier and Grant 1965, Zann 146. 1980, Moosleitner 2002, Kolm and Berglund Bauer, J. C. 1976. Growth, aggregation, and 2003). Kolm and Berglund (2003) determined maturation in the echinoid, Diadema antil- that densities of Pterapogon kauderni were larum. Bull. Mar. Sci. 26:273–277. positively correlated with aggregations of Di- Bednarski, M., and A. Morales-Ramı´rez. adema setosum in Sulawesi, indicating that the 2004. Composition, abundance and distri- urchins formed an important habitat for the bution of macrozooplancton in Culebra fish, which are under strong extraction pres- Bay, Gulf of Papagayo, Pacific coast of sure from the aquarium trade. Those authors Costa Rica and its value as bioindicator of concluded that these aggregations have an pollution. Rev. Biol. Trop. 52 (Suppl. 2): important conservation value for the fish be- 105–118. cause they provide a refuge. Based on the ev- Birkeland, C. 1989. The influence of echino- idence from other regions of the world, the derms on coral-reef communities. Pages aggregations of Astropyga pulvinata in Bahıá 1–79 in M. Jangoux and J. M. Lawrence, 590 PACIFIC SCIENCE . October 2008

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