Reconstruction of Diadema mexicanum bioerosion impact on three Costa Rican Pacific coral reefs

Juan José Alvarado1,2, Jorge Cortés1,3 & Héctor Reyes-Bonilla4 1. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Universidad de Costa Rica, San Pedro, 115012060 San José, Costa Rica; juanalva76@yahoo.com; jorge.cortes@ucr.ac.cr 2. Posgrado en Ciencias Marinas y Costeras, Universidad Autónoma de Baja California Sur, La Paz, México. 3. Escuela de Biología, Universidad de Costa Rica. 4. Departamento de Biología Marina, Universidad Autónoma de Baja California Sur, La Paz, México; hreyes@uabcs.mx

Eastern Tropical Pacific (ETP) reefs are thin CaCO 3 accumulations in relation to their counterparts from the Indo-Pacific and Caribbean (Cortés 1997, Manzello et al. 2008).Most are relative small (1-2 ha), discontinuous, limited to shallow depths (10 m), built by few species, ephemeral in geological time (with low rates of carbonate production but fairly rapid framework accumulation), low cemetation, and have complex food webs (Glynn 1977, Glynn & Macintyre 1977, Macintyre et al. 1992, Cortés et al. 1994, Cortés 1997, Glynn 2004, 2008, Manzello et al. 2008).Two main types of reef structures can be observed in the region (Cortés 1997(Cortés , 2003)): reefs in Mexico, Panama, Colombia and some areas in Costa Rica and Ecuador are built by species of the genus Pocillopora.The other type of reef consists of Porites lobata or Pavona clavus massive corals, with the best developed being at Cocos, Clipperton and Galapagos islands.
After the 1982-83 El Niño event in Cocos Island, Guzman and Cortés (1992) predicted that coral recovery was going to take centuries due to the high densities of bioeroders and the low coral reproduction rates.Guzman andCortés (1992, 2007) indicated that part of the deterioration of the reef structures on Cocos island was due to the bioerosive action of Diadema mexicanum A. Agassiz, 1863.In 2002, there was a five-fold increased of coral cover and a notable reduction in sea urchins.Guzman & Cortés (2007), determined that D. mexicanum was not playing a relevant role in the reef bioerosion.However, the urchin still could fulfill its key role in assisting the recruitment of corals, as has been observed in other reefs in the Caribbean (Sammarco et al. 1974, Sammarco 1980, 1982a, b, Mumby et al. 2006).
We reconstruct the behavior of the bioerosion and bioacretion rates on the reef at Cocos and Caño islands and from Culebra Bay from 1980 until 2009, using published and field information of coral cover, growth and skeletal density, as well as population densities and daily carbonates ingestions of D. mexicanum.Our goal was to understand the role that D. mexicanum plays in the balance of reef growth and destruction through time
Three 10 m long and 1 m wide transects were deployed parallel to the coast, between 4 and 8 m deep.A 1 m 2 quadrat, divided into 0.01 m 2 cells was placed every meter, on the right side of the transect line (Weinberg 1981).The amount of live, dead, and bleached coral cover, and also macroalgae, crustose coralline algae, rocks and sand cover were determined for each quadrat.In addition, sea urchin (D. mexicanum) abundances were counted along the 20m 2 belt transect.
To determine the bioerosion rate per locality (removal of CaCO 3 per time unit), 30 sea urchins were collected (between 08:00 and 10:00 hours) and placed in plastic buckets (5 l), leaving them to evacuated the gut content for a period of 24 hours (Glynn 1988, Reyes-Bonilla & Calderón-Aguilera 1999).The evacuated material was collected and later dried in an oven at 60ºC for 24 h.The samples were weighted on an analytic balance (0.0001 g) and transferred to a furnace at 500ºC for 6 h.After this period, the samples (ashes) were measured again.The difference between the weights determined the amount of organic matter that is present in the sea urchin's gut (Carreiro-Silva & McClanahan 2001).The remaining portion represents the inorganic fraction, composed by CaCO 3 and non-soluble residues (silica fragments like quartz grains, sponge spicules, diatoms, radiolarians and lime).Inorganic fractions were digested with 10% HCl.The remaining material, after dissolution of the carbonates, was filtered with a pre-weighed fiberglass filter.The weight of the residue material retained on the filter corresponds with the non-carbonate fraction (NCF).The difference between the ashes and the weight of the residue equals the CaCO 3 (Carreiro-Silva & McClanahan 2001).This gives us the amount of carbonates removed by each sea urchin (CaCO 3 g ind -1 d -1 ).
The bioerosion rates per urchin (kg m -2 y -1 ) at the different study areas were calculated by multiplying the daily carbonate content (CaCO 3 g ind -1 d -1 ) by density of the sea urchins (ind m -2 ) over 365 days (modified from Carreiro-Silva & McClanahan 2001).
To obtain the carbonate deposition rate of the coral, we used the method proposed by Chave et al. (1972), which combines the coral growth rate (cm y -1 ) and the coral skeletal density (g cm -3 ) to calculate the gross carbonate production.We multiplied this result by the amount of live coral cover (LCC) to estimate the net deposition of carbonates on the reef (CaCO 3 kg m -2 y -1 ).
To obtain the skeletal and coral growth rates, we sampled 10 fragments of colonies of Porites lobata from Cocos Island, five of P. lobata from Caño Island, five of Pocillopora elegans from Caño Island, and five of P. elegans from Culebra Bay.The samples were sent to the laboratory of Ecología Marina, Centro de Investigación Científica y Educación Superior de Ensenada (CICESE), Baja California, México, where the Carricart-Gavinet and Barnes (2007) protocol was applied to obtain density values.The values for coral growth were taken from the literature (Guzman & Cortés 1989, Jiménez & Cortés 2003).For Cocos Island, 10 colonies were stained with Alizarin Red (Lamberts 1978) in August 2007, removed in September 2008, then sliced, measured and the growth rate calculated.
To reconstruct the carbonate budgets, we assumed that coral growth and skeletal density were the same for all the analyzed years, as well as the carbonate content present in the sea urchin's guts.Coral growth can varied between years or seasons, so our reconstruction assumed an "ideal scenario" to asses only the impact of D. mexicanum on reef accretion.To determine the past bioerosion rates, we used literature information about historical D. mexicanum densities (Guzman 1986, Guzman & Cortés 1992, 2007, Lessios et al. 1996, Jiménez 1998, Alvarado & Chiriboga 2008, J.J. Alvarado unpubl.data) and present densities.In addition, to determine past bioacretion rates, we used historical live coral cover information (Guzman et al. 1987, Guzman & Cortés 1992, 2007, Jiménez 2001, J.J. Alvarado & J. Cortés unpubl.data), and present covers.The carbonate balance is a quantitative measured of the functional state of the reef (Perry et al. 2008).As used here, balance refers to the net carbonate budget change in each reef system by comparing the production and the erosion.It is positive if the reef is growing and negative if the reef is eroding (Eakin 2001).
Finally, we analyzed the relationship between D. mexicanum density and the results of reef balance with a logarithmic regression.The regression equation was used to calculate possible scenarios of reef balance in Culebra Bay at different urchin densities (3, 4, 5 and 11 ind m -2 ).

RESULTS
Table 1 displays: 1) carbonate amounts present in the D. mexicanum's gut, and 2) coral growth and skeletal density for the main reefbuilder species.The highest amount of carbonate present in the urchin guts was at Cocos Island, and lowest at Caño Island (Table 1).Pocillopora elegans possesses a higher growth rate than Porites lobata (Table 1).Coral skeletal density was similar in the three study areas, being higher at the species level for P. lobata than for P. elegans (Table 1).
At Cocos Island, we observed a reduction of D. mexicaum density from 1987 to 2009, and a gradual increase in live coral cover (Table 2, Fig. 2A).At this island, the highest sea urchin densities were reported (11.4 ind m -2 ) in 1987,  2).In the three study areas, live coral cover was high (~20-50%) during times when urchin densities were low (< 1 ind m -2 , except for Caño in 1984), and low (~3%) when the densities of D. mexicanum were close to 3 ind m -2 (Table 2).From the three study areas, Caño Island maintained a relatively constant coral cover and urchin density, except that coral cover decreased in 1984, with a slight increase in D. mexicanum density (Table 2).
Finally, in Culebra Bay the carbonate balance was highly positive, with bioacretion rates of 18 kg m -2 y -1 and low bioerosion rates (0.07 kg m -2 y -1 ) until 2006.After that date, there was a drastic change in the carbonate budget, becoming almost negative by 2009 (0.43 kg m -2 y -1 ; Fig. 2C).The bioerosion rate increased from 0.07 to 0.75 kg m -2 y -1 , as a result of the increase in sea urchin density (Fig. 2C).Loss of coral cover (Table 2) resulted from the proliferations of harmful phytoplankton that caused high mortality in the area (Jiménez 2007, Jiménez et al. in prep).
The relationship between D. mexicanum density and reef carbonate balance is negative (Fig. 3).When there are few sea urchins, carbonate balance is highly positive (Culebra Bay: 1996 and2006).When the density of sea urchins exceeds ~1.5 ind m -2 , reef balance start to be negative, becoming highly erosive when urchin density exceeds 4 ind m -2 .Figure 3 help to explain how quickly can be a negative process, such as in Culebra Bay, where in less than 3 years there was a fast loss on reef balance.Also, this analysis help to visualized the slow process of recovery took Cocos Island after a strong disturbance until now days.In the case of Caño Island, it seems that D. mexicanum does not possess a key role in reef balance.For Culebra Bay, a continuing increase in sea urchin density will produce a negative balance.The 2009 densities were 2.19 ind m -2 , pushing the reefs near negative balance.An increase to 3 ind m -2 would produce a considerable reduction on reef erosion, and an increase to 11 ind m -2 would produce a similar impact to reef balance as the one seen in Cocos Island after the 1982-1983 El Niño event.
DISCUSSION Guzman and Cortés (2001) observed that after severe disturbance, the recovery of ETP reefs has been slow, due to the lack of recruitment and the continuous predation by corallivorous organisms.In the case of the 1982-83 El Niño, the recovery was limited by 1) the extreme oceanographic conditions of the region, 2) the high coral mortality suffered during the El Niño, 3) the intense herbivory resulting from high sea urchin concentrations produced high rates of bieorosion, 4) low abundance of recruits due to reduced sexual activity of the main reef builder species, and 5) low potential for successful recruitment due to the low abundance of crustose coralline algae (Guzman & Cortés 2001).Baker et al. (2008) indicated that, for a reef affected by bleaching to recover, a change in the balance between reef accumulation and erosion, the ability to maintain healthy levels of herbivory, and macroalgae cover and coral recruitment are required.
After the 1982-83 El Niño, there was a high incidence of coral mortality and bleaching at Cocos Island.During this period there were high sea urchin densities (Guzman & Cortés 1992), producing a negative carbonate budget, and reef erosion in 1987.It took approximately 15 years for those reefs to switch back to a positive balance.Probably, as Guzman and Cortés (2007) indicated, the impact of the sea urchin as bioeroder declined, and its action as a herbivore facilitated coral recruitment.Thus, the role of the sea urchin can change in accordance with its density.Glynn et al. (2009) indicated a similar recovery pattern for the coral reefs at Darwin  3. Relación logarítmica entre la densidad de Diadema mexicanum (ind m -2 ) y el balance arrecifal (kg m -2 y -1), indicando predicciones de escenarios de balance arrecifal negativo para Bahía Culebra si la intensidad de los disturbios continúan con densidades de 3, 4 y 11 erizos m -2 .Los años indicados en la figura corresponden con las fechas de muestreo de cada área de estudio.Island, northern Galapagos Archipelago, which underwent lower bioerosion in comparison with other reefs in the Archipelago (Glynn 1988).This resulted in an intact reef framework and, together with successful sexual and asexual coral recruitment (Glynn et al. 2009), there was a similar recovery as observed at Cocos Island.The recovery in reef balance observed at Cocos Island, like at Darwin Island, could be due in part to the positive role that Diadema can have through creating spaces for settlement (Carleton & Sammarco 1987) and increasing the cover of crustose coralline algae, which enhances successful settlement (Morse et al. 1988).Vance (1979) found that the sea urchin Centrostephanus coronatus, a member of the Diadematidae family, avoids consuming crustose coralline algae when eating other algae, favoring development of coralline algae.Nevertheless, the sea urchin in search of its food can erode the substrate simply by scraping areas where algae grow (Toro-Farmer 1998).Therefore, in the case of Cocos Island, the herbivorous activity of D. mexicanum possibly resulted in a larger abundance of calcareous algae, and a greater availability of substrate for recruitment of new coral recruits, favoring its recovery.Eakin (2001) indicated that the reef budget in Uva Island, Panama, between 1985 and 2000, was negative, without showing signs of recovery.In some places the densities of Diadema diminished due to the reduction in the reef complexity due to the urchin's erosion, diminishing their refuge.In Cocos Island, reef complexity has remained high (Alvarado et al. in prep.), but density of sea urchins has diminished (Fig. 2A, Table 2), which is probably related to predation.This island has been a no-take Marine Protected Area for the last 30 years, and protection has been strictly enforced for the last 10 years.This has favored the recovery of trophic webs.This contrasts with Panama, where the reefs were under strong fishing pressure for many years, diminishing the presence of predators on D. mexicanum.It has been observed that inside marine reserves, where the fishing pressure has been reduced, the trophic interactions are re-established between the sea urchins and their predators (McClanahan et al. 1999), as opposed to places where intense fishing is occurring and densities of Diadema are high (Harborne et al. 2009).
In Culebra Bay, bioerosion increased after 2009, when a massive explosion of D. mexicanum occurred.The reefs from this area underwent intense mortality due to recurrent proliferations of phytoplankton between 2006 and 2009; these produced intense bleaching resulting from the anoxic conditions of the water and the lack of sun light penetrating to the bottom (Jiménez et al. en prep.).Dead corals were replaced by turf algae.This availability of algae could have caused an increase in the recruitment of sea urchins, increasing their densities, and their bioerosional effect.If this bioerosion continues, the coral framework will be weakened and may collapse (Colgan & Glynn 1990).Figure 4 illustrates the difference in conditions in 2005 compared to now.
Bioerosion intensity depends on several environmental factors, like depth, light and nutrient supply (Chazottes et al. 1995).Baker et al. (2008) indicated that a variety of disturbances can cause a significant reduction in live coral cover.Eutrophication, sedimentation and bleaching can quickly initiate to an erosive phase, resulting in a loss of structural integrity and topographical relief.Moreover, Edinger et al. (2000) mentioned that coral reefs growing in eutrophic coastal environments are exposed to higher bioerosion than those in clear oceanic waters, resulting in negative carbonate budgets.In Dominican Republic, Tewfik et al. (2005) found that a nutrient enrichment together with overfishing accelerated the environment deterioration, and facilitated an increase in sea urchin densities (Lytechinus variegatus).As consequence of this population increase there was a considerable reduction on the diversity on the affected areas.
In Culebra Bay, the environmental conditions have deteriorated in recent years due to anthropogenic eutrophication (Fernández 2007, Fernández et al. in prep.).This has resulted in invasions by Caulerpa sertularoides (Fernández & Cortés 2005, Fernández 2007) and phytoplankton proliferations (Jiménez 2007, Jiménez et al. in prep.).As a consequence, live coral cover in the Bay has declined (Jiménez 2007, Bezy et al. 2006, Cortés et al. 2010, Fernández et al. in prep.).When nutrients become abundant, reef carbonate producers tend to be overgrown by fast-growing fleshy and filamentous algae.Meanwhile the bioeroders tend to increase due to the food availability, magnifying the negative effects (Chazottes et al. 1995).Additionally, successful recruitment by juvenile sea urchins have been attributed to algal proliferation because of the increase in nutrient availability, favoring a greater density of sea urchins in organically enriched areas (Eklöf et al. 2008).
Another negative factor that could have promoted an increase in D. mexicaunm high densities at Culebra Bay, is that this area suffers from a strong fishing pressure, with few controls and complete lack of protection of the resources.With few or no sea urchin predators and with more food available, Diadema reached densities never before reported for the area (Table 2), causing an increase in bioerosion of the coral framework.On Marías Island in Mexico, and in the Canary, Galapagos and Hawai'i archipelagos, it has been observed that reductions in the populations of predator fishes by overfishing resulted in an increase in sea urchin abundance (Torrejón-Arellano et al. 2008, Clemente et al. 2009, Sonnenholzner et al. 2009, Vermeij et al. 2010).
According to Muthiga and McClanahan (2007) it is of interest to record the historical level of the Diadema populations, as it may indicate the degree to which the sea urchin are required for the maintenance of the coral reef ecology or a negative factor that has been released from predation by overfishing.Through the reconstructions presented here (Fig. 2), it is possible to visualize how Diadema mexicanum can have either a positive or a negative effect on coral reef development in the Eastern Tropical Pacific.Moreover, it was shown that for the sea urchin to have a positive or negative role, a series of synergies are required to switch it in one direction or another.Bad coastal management (anthropogenic eutropfication) and overfishing (lack of sea urchin predators), can result in this sea urchin eroding the coral framework, as seen in Culebra Bay.However, where the trophic webs are "healthy", Diadema mexicanum facilitates the growth of crustose coralline algae, which at the same time helps the recovery of coral cover.As Veron et al. (2009) pointed out, "a reef far from additional human stress can realize a rapid recovery, returning to its own diversity in less than a decade".Cocos Island, is an example of this statement, while Culebra Bay, being subjected to additional stress, likely will take longer to recover.MPAs provide the means for effectively limiting the number of urchins on coral reefs and subsequently returning the calcium carbonate cycle to a more balanced state (Brown-Saracino et al. 2007).However, if the anthropogenic eutrophied conditions diminish, there is fishery management, and there is stronger protection of the reef environments, it is possible that Diadema can help in the recovery of those reefs.To assess the future development of reef structures and their relationship with sea urchins it is important to continue monitoring the populations on all of these reefs.However, it is currently extremely important to do this in Culebra Bay, so that management measures can be initiated if D. mexicanum attain densities of > 3 ind m -2 .Also, it is extremely important to begin studying recruitment and reproduction patterns, as well as to initiate efficient coastal and fishery management practices.Glynn and Fong (2006) stated that if corals survive total mortality and if environmental conditions return to pre-disturbance levels, there exits the potential for rapid coral recovery in a few years.For Culebra Bay, this statement is extremely important, because its highlight the need for a better coastal management that would improve coastal ecosystems and their services.