Bomb-cratered coral reefs in Puerto Rico, the untold story about a novel habitat: from reef destruction to community-based ecological rehabilitation
Los arrecifes de coral con craters-bomba en Puerto Rico, la historia no contada sobre un hábitat inusual: desde la destrucción de arrecifes hasta la rehabilitación ecológica basada en la comunidad
Edwin A. Hernández-Delgado1*,2*, Alfredo Montañez-Acuña1,2, Abimarie Otaño-Cruz1,2 & Samuel E. Suleimán-Ramos2
Abstract
Ecological impacts of military bombing activities in Puerto Rico have often been described as minimal, with recurrent allegations of confounding effects by hurricanes, coral diseases and local anthropogenic stressors. Reef craters, though isolated, are associated with major colony fragmentation and framework pulverization, with a net permanent loss of reef bio-construction. In ]]>
Acropora cervicornis farming. Reef craters ranged in size from approximately 50 to 400m2 and were largely dominated by heavily ]]>
A. cervicornis into formerly bombarded grounds have proved successful in increasing percent coral cover, benthic spatial heterogeneity, and helping rehabilitate nursery ]]>
Key words: Benthic community structure, bombing impacts, community-based ecological rehabilitation, coral reefs, fish community structure, military activities, novel habitats.
Resumen
Los impactos ecológicos de las actividades militares de bombardeos en Puerto Rico se han descrito a menudo como mínimos, con recurrentes denuncias al confundir efectos por huracanes, enfermedades de corales y estresores antropogénicos locales. Los cráteres de arrecife, aunque aislados, están relacionados con una alta fragmentación de la colonia y pulverización ]]>
Acropora cervicornis. Los cráteres de arrecife se distancian en tamaño de aproximadamente 50 a 400m2 y fueron dominados ampliamente por fragmentos de bentos aplanado, con una cubierta de coral generalmente por debajo de 2% y el predominio de ]]>
A. cervicornis en terrenos anteriormente bombardeados han demostrado un éxito al aumentar el porcentaje de cobertura de coral, la heterogeneidad espacial bentónica y ayudando a rehabilitar funcionalmente la tierra para vivero.
Palabras clave: estructura de la comunidad bentónica, impactos de bombardeo, rehabilitación ecológica basada en la comunidad, ]]>
Long-term adverse ecological impacts of military maneuvers on coral reef ecosystems have remained as a concern as there is still limited information in the literature about impacts across multiple spatial and temporal scales. Most studies have ]]>
Localized bombing impacts on coral ]]>
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Reef craters present in both, Culebra and Vieques Islands coral reefs are often very small in comparison to the scale of each island, each ranging in size from approximately 50 to 400m2. But these are largely dominated by heavily fragmented flattened benthos, with % coral cover usually below 2% and dominance by non-reef building taxa (i.e., filamentous algal turfs, ]]>
Fig. 1a-c). In contrast, adjacent non-bombarded reef zones are still dominated by consolidated benthos, with higher percent living coral cover and larger abundance of reef building species (Fig. 1d-f). Benthic spatial heterogeneity is also significantly lower within crater scales which also results in a lowered functional value as fish nursery ground. The fact that physical disturbance within bombarded grounds was so locally extensive resulted in a mosaic of habitat patches with permanent loss of reef framework and in potentially declining multiple ]]>
de facto novel habitat, and as such, there is a need to address the ecological status of benthic and fish communities, as well as their recovery state three to five decades after bombing.
This study was aimed at: 1) documenting the condition of benthic communities within 35-50 year-old ]]>
Acropora cervicornis (Lamarck, 1816), and rehabilitate bombarded coral reefs.
Materials and Methods
Study sites: Studies were conducted across 15 fringing reef sites, 11 at Culebra Island (located between 18°19.791’N, 65°19.943’W and 18°20.776’N, 65°20.498’W) ]]>
Fig. 2). Reef craters examined in this study ranged between 50 and 400m2. Sites were selected based on their representativeness of typical reef segments impacted by framework destruction as our aim was documenting what is the status of ]]>
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Benthic community: Benthic habitats were characterized across all sites through 3-6 replicate ten m-long digital video-transects. Number of replicates varied as a function of crater size and covered at least 50-75% of the impacted area within each crater. Transect deployment within each crater was haphazard, often separated by at least 5m. A total of six random, non-overlapping still images/transect were obtained and analyzed with Coral Point Count with excel extensions (v3.6) (Kohler & Gill, 2006) to address percent cover of all benthic components, including coral, algal ]]>
Halimeda spp.), cyanobacteria, other components, sand, rubble, and bare substrate. A total of 20 random dots per image were used. Coral species richness, species diversity index (H’n) (Shannon & Weaver, 1948), and evenness (J’n) (Pielou, 1966) were also calculated.
Coral recruits: Coral recruit ]]>
Fish community structure: Fish communities were characterized only in Culebra using stationary visual censuses within craters (impacted) and adjacent (control) locations following a slight modification from Bohnsack and Bannerot, (1986). Data was collected within a 5 m-radius imaginary cylinder during a period of 15min. All individuals were counted, identified to the lowest taxon possible, and standard fork length was estimated. Size data were used to estimate biomass. Weight-length relationships were calculated following Bohnsack and Harper (1988). Basic information of the fish community structure reported in this study included species richness, ]]>
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Statistical analyses: A three-way permutational analysis of variance (PERMANOVA) was used to test the null hypothesis of no significant difference in benthic biodiversity parameters and community structure between sites (Culebra, Vieques), treatment level (bombarded areas, non-impacted controls), and depth (1-3m, 6-9m) using PRIMER-e v.6.1.14 (Anderson, Gorley & Clarke, 2008). Principal component ordination (PCO) was used to determine which benthic taxa explained spatial clustering patterns of benthic communities. Proportional data on percent benthic components cover were ]]>
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Coral reef rehabilitation: A total of 2 000 corals were harvested from existing low-tech coral farms through the Community-Based Coral Aquaculture and Reef Rehabilitation Project and outplanted to adjacent coral reefs within former military maneuver ranges at two sites in Culebra Island, Bahía Tamarindo and Punta Soldado. Sites selected for outplanting were located within a flat shallow reef (<2.5m) used as artillery maneuver areas at ]]>
m2. Survival rates and growth were addressed following two representative patches located at elevated rocky outcrops and two patches adjacent to reef sand pockets at increasing time intervals during a year. A two-way ANOSIM was used to test the null hypotheses of ]]>
Results
Benthic community: Coral reef ]]>
Table 1). There was a significantly different benthic community structure between sites (p=0.0473) and treatments (p=0.0348). Also, interactions between site and treatment, treatment and depth, and among site, treatment and depth were highly significant. Bombarded sites were characterized by having significantly lower coral species richness (p=0.0452), percent coral cover (
p=0.0025), H’n (p=0.0107), and J’n (p=0.0174) (Fig. 3a-d). Mean coral species richness within bombarded bottoms was 2.2/transect, while mean ]]>
Fig. 1e-f). But none of these differences were significant.
The percent relative cover of the most important reef building coral species was significantly lower within bombarded areas (Fig. 4). Montastraea(=Orbicella) annularis ]]>
O. faveolata (Ellis & Solander, 1786), O. franksi (Gregory, 1895), and M. cavernosa Linnaeus, 1767 averaged 1.3, 0.5, and 1.0%, respectively, at control sites. None of these species were present within bombarded areas. Colpophyllia natans (Houttuyn, 1772) averaged 0.01% within bombarded grounds and ]]>
Diploria strigosa (Dana, 1846) averaged 0.7% at control sites and was absent within bombarded areas, and Siderastrea siderea (Ellis & Solander, 1786) had a mean 0.14% cover within bombarded areas and 1.8% in control sites.
Principal component ordination (PCO) analysis showed two larger clusters of reef communities, and 5 individual sites (Fig. 5). Impacted sites at Culebra were dominated by open substrates composed by a mixture of bare bedrock, rubble and sand pockets (SPR), algal turf, brown macroalgal patches (e.g., Dictyota spp.), and sporadic colonies of octocoral Pseudopterogorgia spp. (Fig. 1a-b). Vieques impacted sites were dominated by algal turfs (Fig. 1c). Culebra control site showed a higher spatial heterogeneity mostly dominated by macroalgae, M. annularis, and P. astreoides (Fig. 1c-d). Control sites at Vieques were also dominated by turf, and in a lesser degree a mixed octocoral community. The proposed PCO solution explained 57% of the observed spatial variation. ]]>
Coral recruits: Coral recruit density was significantly higher (PERMANOVA, Pseudo-F=6.55, p=0.0001) within non-impacted control sites in comparison to bombarded areas. Control site CR-C1 located within CLPNR averaged 51 colonies/30m2, while CR-C2 outside CLPNR averaged 21 colonies/30m2 (Fig. 6). Impacted site CR-I1 averaged 8 colonies/30m2, while CR-I2 averaged less than 3 colonies/30m2. Both impacted sites were also located within CLPNR. ]]>
p=0.0001). Also, species richness (R=0.736, p=0.0006), and H’n (R=0.747, p=0.0006) were significantly higher at control sites than at bombarded areas. No significant difference in J’n was documented. Brooder species such as Favia fragum (Esper, 1795), Siderastrea radians (Pallas, 1766), and Porites astreoides (Lamarck, 1816) were dominant at control sites, while lower abundances of S. radians and P. astreoides ]]>
Fig. 7). The three clusters composed of control non-impacted sites were explained by P. astreoides, P. porites, F. fragum, and Millepora striata (Lamarck, 1816). Bombarded sites clusters were determined by S. radians. The ]]>
Fish community: Fish community structure also showed significant difference (p<0.0001) between treatment levels that were mostly related to a highly significant decline (p=0.0030) observed in the reef structural heterogeneity index (RSHI) within bombarded sites (Fig. 8a). RSHI had a mean value of 0.69 within bombarded areas and 2.72 within control sites. Fish species richness was significantly higher (23.4 per count) at control sites (p=0.0020) than at bombarded areas (12.6) ]]>
Fig. 8b). Fish abundance was also significantly higher (p=0.0002) at control sites (491) versus bombarded sites (108) (Fig. 8c). Also, H’n was significantly higher (p=
0.0020) within control areas (1.6744) in comparison to bombarded grounds (1.1716) (Fig. 8d). Total fish biomass was significantly higher (p=0.0001) at control sites (7 697g) than at bombarded areas (999g) (Fig. 8e). Similarly, piscivore biomass was significantly higher ]]>
p=0.0002) at control sites (2,406 g) than at bombarded areas (206g) (Fig. 8f). All fish community parameters showed a highly significant linear regression (p<0.0088) with RSHI (Table 2), suggesting the strong permanent negative impacts of bombing activities on the demolition of reef framework and the net decline in fish communities ]]>
Scarus iserti Bloch, 1790, S. vetula Schneider, 1801, Sparisomq viride (Bonnaterre, 1788), S. rubiprinne (Valenciennes, 1839), and S. radians (Valenciennes, 1839), and browsers such as Acanthurus coeruleus ]]>
Epinephelus guttatus (Linnaeus, 1758), E. adscensionis (Osbeck, 1765), Cephalopholis fulva (Linnaeus, 1758), and C. cruentata (Lacepède, 1802), and snappers Lutjanus jocu (Schneider, 1801), L. analis (Cuvier, 1828), and L. apodus ]]>
Coral reef rehabilitation: Mean percent colony survival rates of Acropora cervicornis outplants was 81% ]]>
Fig. 9). Percent survival at elevated rocky outcrops reached 92% at impacted sites and 84% at control sites. Percent live coral tissue cover on outplanted colonies averaged 85% at both, impacted and control sites after one year (Figure 10a), ranging from 82 to 88% within impacted sites in low-relief ]]>
Figure 10b). Total outplanted colony branch abundance/colony showed a mean overall increase from 4.5 to 14.4 cm across impacted sites, and from 3.4 to 8.3cm across control ]]>
Figure 10c). Temporal effects were significant for all variables, but treatment and position effects were not (Table 3).
Discussion
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Profound, acute and persistent negative impacts of historical bombing activities were documented in Culebra and Vieques Islands, Puerto Rico, across coral reef craters spatial scales. Severely impacted reef segments were characterized by having significantly lower spatial relief, bedrock exposure and an abundant mixture of unstable turf-covered rubble and bedrock boulders demolished by explosions. These substrates were also characterized by low coral colony abundance, low percent living coral cover, low coral species richness and H’n, when compared to adjacent control sites. ]]>
M. ]]>
species complex, implies that at the local ecosystem scale, bombarded coral reefs have shown a permanent shift in composition and functions, that full recovery of previously existing benthic community structure and spatial heterogeneity may take centuries. Coral recruitment rates of critical reef-building species across the northeast Caribbean region are increasingly low (Rogers, Fitz, III, Gilnack, Beets & Hardin, 1984; Edmunds & Elahi, 2007; Edmunds, Ross & Didden, 2011), suggesting that habitat fragmentation by bombing has resulted in a permanent localized loss of coral reproductive stock and that in ]]>
Bombarded areas were also characterized by sustaining lower fish species richness, H’n, abundance, and biomass, as a result of the permanent loss and lack of recovery of reef benthic spatial relief. They also had a very low abundance or absence of significant fish functional groups of ]]>
Individual reef craters are often small in size (50-400m2) and isolated in space, which render them as very small spatial units generally disregarded as having low ecological ]]>
M. annularis growth rates on individual coral core samples from Vieques, but Macintyre, Raymond & Stuckenrath (1983) found significant destruction by bombing of shallow Acropora ]]>
(Lamarck, 1816) and Porites porites (Pallas, 1766) frameworks. Porter et al. (2011) also found a statistically significant inverse correlation between the coral species richness, colony abundance and species diversity, and the density of military ordnance across reef scales in Vieques. Nonetheless, at smaller ecological scales (e.g., fringing reef unit), reef craters represent localized mosaics of reef segments that were severely reduced to a flattened, unstable, demolished reef bottom, with depauperate biodiversity, that have shown little or no recovery even ]]>
The lack of meaningful natural coral reef recovery within 35-50 year-old reef craters from Culebra is alarming, but surprisingly, still poorly addressed. Our study suggests ]]>
S. radians and P. astreoides. There is increasing evidence that natural coral reef recovery ability from blasting even across small spatial scales can become severely limited with increasing spatial and temporal scale of destruction. Extensively blasted areas for fishing in Indonesia showed no significant recovery within a period of six years despite adequate coral larval supply from adjacent reefs (Fox & Caldwell, 2006). ]]>
A particular concern is that a habitat once dominated by a M. annularis species complex framework has not shown any sign of recovery over the course of several decades through sexual coral larval recruitment. Though coral larval settlement do occur within the crater, coral spat mortality appears to be high largely due to the unstable fragmented nature of the bottom. Considering the significant decline of M. annularis
species complex percent living cover across the region (Miller et al., 2009; Hernández-Pacheco et al., 2011, Edmunds, 2013), recovering benthic spatial heterogeneity ecological functions is largely improbable. Therefore, an alternative strategy that can potentially achieve rapid results in rehabilitating shallow reef ecological functions as juvenile fish nursery grounds is the use of community-based, low-tech farming and outplanting of rapid-growing Acropora cervicornis. Low-tech, community-based approaches to culture, harvest and transplant A. cervicornis into formerly bombarded grounds proved highly successful in fomenting increasing benthic spatial heterogeneity, while fostering meaningful community-based participation. Outplanted colonies showed outstanding survival and growth rates. Observed decline occurred as a result of partial coral ]]>
Coralliophila abbreviata Lamarck, 1816 and C. caribaea Abbott, 1958, and by fireworm Hermodice carunculata Pallas, 1766; in comparison to adjacent controls outside the reserve. This could be the result of lack of invertebrate predators across control ]]>
A. cervicornis farming and outplanting is a key successful tool to help rehabilitate shallow reef nursery grounds. But further, it also showed that reef trophic condition is a key element in determining reef rehabilitation success. Therefore, the combination of a no-take marine protected area designation and low-tech ]]>
There is also a concern that military impacts on coral reef are ecologically persistent and that they may still represent a risk of toxic pollution further threatening reef recovery. Goenaga (1986, 1991) suggested that the large abundance of unexploded ordnance and the potential leaching of pollutants from ]]>
Our findings showed that there was still an untold story about bombing impacts across small reef spatial ]]>
de facto novel habitat. Natural reef recovery abilities within bombarded reefs need to be continuously monitored. Targeted monitoring efforts will become critical in the context of increasing sea surface temperature and its long-term impacts on coral reefs. Declining reefs across the region due to climate change impacts may aggravate the ability of bombarded reefs to show at least a modest degree of recovery. The lack of natural recovery ability coupled ]]>
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Acknowledgments
This study was possible thanks to the support provided to E.A. Hernández-Delgado by the National Science Foundation HRD #0734826 through the Center for Applied Tropical Ecology and Conservation. We also thank the partial support from the Caribbean Coral Reef Institute of the University of Puerto Rico ]]>
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1. University of Puerto Rico, Center for Applied Tropical Ecology and Conservation, Coral Reef Research Group, PO Box 23360, San Juan, PR 00931-3360; fax: 1-787-764-2610; edwin.hernandezdelgado@gmail.com, omsjulio@hotmail.com, alfredo.a.montanez@gmail.com, abimarie07@gmail.com
2. Sociedad Ambiente Marino, PO Box 22158, San Juan, PR 00931-2158; samuelsuleiman@gmail.com
Received 23-VIII-2013 Corrected 21-II-2014 Accepted 24-III-2014
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