Reconstruction of Diadema mexicanum bioerosion impact on three Costa Rican Pacific coral reefs
Juan José Alvarado1*,2*, Jorge Cortés1,3* & Héctor Reyes-Bonilla4*
*Dirección para correspondencia Abstract ]]>
The 1982-83 El Niño event produced a high coral mortality (50-90%) in several localities in the Eastern Tropical Pacific, which resulted in an outbreak of the sea urchin populations of Diadema mexicanum A. Agassiz, 1863 in some reefs, leading to an increase in coral framework bioerosion. In Costa Rica, El Niño impact varied ]]>
D. mexicanum densities followed the same pattern. To understand the historic role of this sea urchin on the balance between bioerosion and bioacretion, we made a reconstruction of bioerosion impact based on current patterns of carbonate ingestion by the sea urchins, growth rates and skeletal density of the main coral builders, and historical information of sea urchin population density and coral cover. The reconstruction model varied depending on locality. At Cocos Island, the ]]>
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Keywords: Density, coral cover, bioerosion, bioacretion, management, reef budget, Eastern Tropical Pacific.
Resumen ]]>
El fenómeno de El Niño de 1982-83 produjo una alta mortalidad coralina (50-90%) en varias localidades del Pacífico Tropical Oriental, lo que en algunos arrecifes trajo como consecuencia una explosión en la poblaciones de erizos de mar, Diadema mexicanum, y por consiguiente un aumento en la bioerosión del basamento coralino. En Costa Rica, el impacto fue diferencial en tres localidades arrecifales, ]]>
D. mexicanum. Con el fin de poder entender el papel histórico que desempeña este erizo de mar en el balance entre bioerosión y bioacreción, se reconstruyó el impacto bioerosivo basándose en patrones actuales de ingestión de carbonatos por parte del erizo, tasas de crecimiento y densidad del esqueleto coralino, y datos históricos de densidad ]]>
Palabras claves: Densidad, cobertura coralina, bioerosión, bioacreción, manejo, balance arrecifal, Pacífico Tropical Oriental. Eastern Tropical Pacific (ETP) reefs are thin CaCO3 accumulations ]]>
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, ]]>
et al. 2008). Two main types of reef structures can be observed in the region (Cortés 1997, 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 ]]>
The Eastern Tropical Pacific has been one of the most affected regions by sea warming as a result of El Niño events (Glynn & Colley 2001), with significant live coral cover losses at most localities (50-100%) due to bleaching (Glynn 1988,1990, 1996, Guzman & Cortés 1992, 2001, 2007, Glynn et al. ]]>
et al. 2001, Baker et al. 2008), which facilitated the growth of macroalgae and increased bioerosion by sea urchins (Glynn et al. 1979, 1988, 1997, Eakin 1992, 1996, 2001, Reaka-Kudla et al. 1996, Guzman & Cortés 1992, 2007). During the 1982-83 El Niño event ]]>
et al. 1987), and death of coral colonies of Pocillopora spp. was observed in Culebra Bay (Cortés et al. 1984). During the 1997-98 El Niño event, the coral reefs of these three localities were less impacted (~5% coral ]]>
et al. 2001), despite the fact that this El Niño was considered to be the most intense one of the last century (Enfield 2001).
After the 1982-83 El Niño event in Cocos Island, Guzman and Cortés (1992) predicted that coral recovery was going to take ]]>
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 ]]>
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 ]]>
D. mexicanum. Our goal was to understand the role that D. mexicanum plays in the balance of reef growth and destruction through time
]]>
Materials and Methods
To reconstruct a reef budget it was necessary to estimated the current bioacretion and bioerosion rates. For this, we visited three reef sites per study area (Fig. 1), where transects to ]]>
Three 10 m long and 1 m wide transects were deployed parallel to the coast, between 4 and 8 m deep. A 1 m2 quadrat, divided into 0.01 m2 cells was placed every meter, on the right side of the ]]>
D. mexicanum) abundances were counted along the 20m2 belt transect.
To determine the bioerosion rate ]]>
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 ]]>
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 ]]>
3 (Carreiro-Silva & McClanahan 2001). This gives us the amount of carbonates removed by each sea urchin (CaCO3 g ind-1 d-1).
The bioerosion rates per urchin (kg m-2 y-1) at the different study ]]>
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 ]]>
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 (CaCO3 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. ]]>
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. ]]>
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 ]]>
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 ]]>
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 ]]>
-2).
Results Table 1 displays: 1) ]]>
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). Pocilloporaelegans 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. mexicanum 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, whereas they were ≤ 1 ind m-2 (Table 2) from 2002 to 2009. At Caño Island, the densities were below 0.50 ind m-2, while in Culebra Bay they increased 900% from 2006 to 2009 (Table 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).
In Cocos Island, as the density of Diadema decreased, its bioerosion impact decreased (Fig. 2A). In 1987, intense bioerosion (9.3 kg m-2 y-1) and very low bioacretion (0.4 kg m-2 y-1) were observed, resulting in a negative balance in the carbonate budget (Fig. 2A). At this locality there was a positive balance in 2002, which was maintained until 2009, with net accretion of 3.1 kg m-2 y-1 (Fig. 2A).
In Caño Island, D. mexicanum had little impact on bioerosion (<1 kg m-2 y-1) in comparison to Cocos Island (Fig. 2A-B). Also, bioacretion has been high (~11 kg m-2 y-1), producing a positive carbonate balance (Fig. 2B).
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 and 2006). 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 ]]>
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 ]]>
]]>
Glynn et al. (2009) indicated a similar recovery pattern for the coral reefs at Darwin 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 ]]>
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 ]]>
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 ]]>
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 ]]>
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 ]]>
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).
At Caño Island, from the historic densities of D. mexicanum (Fonseca 1999, Guzman & Cortés 2001, Fonseca et al. 2006), it seems that this sea urchin has not been an important bioeroder and that its impact has been minimum (Fig. 2B). Scott et al. (1988) ]]>
-2 y-1). Later, in 1996, Fonseca (1999) determined a lower bioerosion rate (0.05 kg m-2 y-1) for Platanillo Reef, as well as high bioacretion (7.1 kg m-2 y-1). Guzman and Cortés (2001) indicated that these reefs in the 1997-98 El Niño had less effect than prior events because of high crustose coralline cover (80-95%) and successful coral recruitment.
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 ]]>
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 ]]>
Bioerosion intensity depends on several environmental factors, like depth, light and nutrient supply (Chazottes et al. 1995). Baker et al. ]]>
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 ]]>
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 ]]>
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, ]]>
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 ]]>
et al. 2008).
Another negative factor that could have promoted an increase in D. mexicanum high densities at Culebra Bay, is that this area suffers from a ]]>
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 ]]>
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 ]]>
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 ]]>
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 ]]>
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 ]]>
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 ]]>
Acknowlegments
We acknowledge the following persons and institutions that collaborate during the development of this work: C. Fernández, O. Breedy, C. Sánchez, S. Martínez, E. Gómez, A. Planas, V. Flores, O. Norzagaray, L.E. Calderón-Aguilera, ]]>
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*Correspondencia a: Juan José Alvarado. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica; juanalva76@yahoo.com. Posgrado en Ciencias Marinas y Costeras, Universidad Autónoma de Baja California Sur, La Paz, México. ]]>
Jorge Cortés. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica; jorge.cortes@ucr.ac.cr. Escuela de Biología, Universidad de Costa Rica. Héctor Reyes-Bonilla. Departamento de Biología Marina, Universidad Autónoma de Baja California Sur, La Paz, México; hreyes@uabcs.mx 1. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Universidad de Costa Rica, San Pedro, 11501-2060 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
Received 23-II-2011. Corrected 05-X-2011.Accepted 29-II-2012.
