Chronic eutrophication and turbidity are critical detrimental factors impacting coral reef ecosystems, adversely affecting their ecological functions, services, benefits, and resilience across multiple spatial scales and over prolonged periods of time. Inadequate land use practices and lack of appropriate sewage treatment can adversely contribute to increase land-based source pollution (LBSP) impacts in coastal waters and to magnify impacts by sea surface warming trends associated to climate change. Fringing coral reefs off Vega Baja, Puerto Rico, support extensive remnant patches of Elkhorn coral Acropora palmata (Lamarck 1816), which was listed in 2006 as a threatened species under the US Endangered Species Act. Chronic impacts by LBSP have significantly affected local downstream fringing reefs. We characterized the spatial extent of a water quality stress gradient across 12 reefs along the Vega Baja coast through monthly measurements of multiple physico-chemical parameters. Most parameters, particularly PO4, , chlorophyll-a, and the concentration of optical brighteners (OABs), showed a statistically significant increase (PERMANOVA, p < 0.05) in waters close to the main pollution sources, but also in waters adjacent to Cibuco River effluents. Dissolved oxygen also declined and turbidity increased on polluted sites. PO4, , and chlorophyll-a, exceeded recommended concentrations for coral reef ecosystems by factors of 7 - 50 times, 600 - 1240 times, and 17 - 83 times, respectively, depending on the source of the effluents and the distance from sewage pollution sources. Also, water turbidity exceeded 4 - 10 times the recommended value for pristine coral reefs. Coral reefs showed significant decline in close proximity to the polluted zone, showing a significantly different benthic community structure (PERMANOVA, p < 0.0001) dominated by non-reef building taxa (i.e., macroalgae, algal turf) and bare substrate. Percent coral cover and abundance of A. palmata, showed a significant increase with distance. Coral species richness, species diversity index, and the variance in taxonomic distinctness were very low on reef patches adjacent to the polluted zone, increased at a moderate distance with increasing coral cover and co-existence of multiple species, and declined far from the pollution source due to dominance exerted by A. palmata. This study suggests that chronic LBSP resulted in a major decline of one of the largest and most dense remnant stands of A. palmata across the northeastern Caribbean and that nutrient and chlorophyll-a concentrations were unsustainable for coral reefs. This situation requires immediate solution to prevent further damage to these unprecedented resources. It further suggests that chronic LBSP may synergistically magnify sea-surface warming impacts driving corals to an increased state of risk in face of forecasted climate change impacts. Actions to mitigate and adapt to climate change impacts on coral reefs must require a priori controls of LBSP to be effective.
Coral reefs are the most diverse and productive marine ecosystems of the world [
Nutrient enrichment is one of the most significant coral reef stressors, in combination with increased Sea Surface Temperature (SST), increasing human population across coastal habitats, and overfishing [
community structure favoring algal growth [
Elkhorn coral, Acropora palmata (Lamarck 1816), is a large branching coral with thick and sturdy antler-like branches, and constitutes a mono-specific coral functional group in Caribbean shallow reef front zones as they provide shelter habitat for multiple species (
Acroporid coral populations have significantly declined over the past four decades across the Western Atlantic as a consequence of the impact of hurricanes, disease outbreaks, local anthropogenic factors and the impact of climate change [
This study documents the impact of chronic LBSP on the ecological status of A. palmata dominated coral reefs along a gradient of impacts on the coast of Vega Baja, PR. The null hypothesis of no significant differences in the status of coral reef benthic community structure along a LBSP stress gradient was tested using various multivariate statistical tests to determine whether these factors individually or collectively have any significant impact on coral reefs.
Water quality sampling took place along the coastal waters of Vega Baja in the northern coast of Puerto Rico
Example of healthy, high-density Acropora palmata stands at Vega Baja, PR. These reefs still largely unknown to science support outstanding densities of this threatened species
(
The ecological condition of 12 coral reef patches was characterized along a suspected water quality stress gradient in the Vega Baja coast (
Water quality sampling sites. Known pollution sources are marked at the Cibuco River mouth, at the eastern side of the existing sand tombolo at Balneario Playa Puerto Nuevo—BAL (public beach), and at the storm water runoff outlet at Plazoleta de los Pescadores—PLA. Acronyms described in Methods. Red polygon represents the benthic community sampling range
Coral reef benthic community sampling design. Eastern inshore: PR-E, PR-W; Eastern offshore: AF-E, AF-W; Mid inshore: PO-E, PO-W; Mid offshore: HI-E, HI-W; West inshore: Eco-In, Eco-Mid; West offshore: Eco-Off-E, Eco-Off- W. Acronyms described in Methods
sewage pollution point source at PLA across three different distance categories: East (<200 m), Middle-MID (200 - 400 m), and West (400 - 700 m). In addition, reefs were subdivided in two segments at increasing distance from the shoreline: inshore (<100 m), and offshore (100 - 250 m). Benthic community sampling sites were subdivided as follows: East-Inshore: Pasarratos-East [PR-E] (18˚29'22.17"N, 66˚24'25.90"W), Pasarratos-West [PR-W] (18˚29'24.35"N, 66˚24'28.44"W), East-Offshore: Afropoint-East [AF-E] (18˚29'29.08"N, 66˚24'30.65"W), Afropoint-West [AF-W] (18˚29'28.96"N, 66˚24'33.41"W); Mid-Inshore: Las Pozas-East [PO-E] (18˚29'24.76"N, 66˚24'34.35"W), Las Pozas-West [PO-W] (18˚29'24.65"N, 66˚24'36.09"W); Mid-Offshore: Hawaii-East [HI-E] (18˚29'29.00"N, 66˚24'44.08"W), Hawaii-West [HI-W] (18˚29'29.05"N, 66˚24'35.37"W); West-Inshore: El Eco- Inshore [Eco-In] (18˚29'24.07"N, 66˚24'39.41"W), El Eco-Mid [Eco-Mid] (18˚29'25.38"N, 66˚24'38.62"W); West-Offshore: El Eco-Offshore-East [Eco-Off-E] (18˚29'28.02"N, 66˚24'38.00"W), El Eco-Offshore-West [Eco-Off-W] (18˚29'28.00"N, 66˚24'39.33"W).
Triplicate samples per parameter were obtained at each sampling site during each visit on a nearly monthly basis for eleven months, from July, 2013 to May, 2014. A total of 13 variables were tested, including water temperature, salinity (ppt), conductivity (mS), and dissolved oxygen concentration (mg/L) with a YSI85 digital data logger. The pH and dissolved nutrient concentrations, including phosphates (PO4), nitrates (NO3), nitrites (NO2), ammonium (NH3 and
Coral reef benthic community structure was characterized across twelve individual coral reef patches located along an increasing east-west distance, and along an inshore-offshore distance gradient from a known pollution source at PLA (
Water quality data was analyzed using a suite of multivariate statistical methods in the statistical package PRIMER v6.1.16 + PERMANOVA v1.0.6 (Plymouth Marine Lab, UK) [
The null hypothesis of no significant difference in coral reef benthic community structure among surveyed sites was also tested using a 3-way PERMANOVA, with distance (n = 3), segment (n = 2), and site (n = 12) as main variables. Also distance × segment, distance × site, segment × site, and distance × segment × site interactions were tested. A similar approach was used to test for S, H’c, J’c, and sΔ+. Spatio-temporal patterns were illustrated following a Bray-Curtis ordination cluster analysis and MDS ordination. PCO was used to identify spatial patterns of coral reef benthic community structure clustering and indicator taxa of such clustering patterns. A combination of linear and non-linear regression models were fit using Sigma Plot v11.0 (Systat Software, Inc.) to test the relationship of individual coral reef taxa and increasing linear distance from the pollution source. In addition, a Spearman rank correlation was carried out between individual coral reef benthic components and individual water quality parameters to test for any significant relationship.
Sea Surface Temperature (SST) was significantly lower (p < 0.0001) at PLA due to the discharges of freshwater from an underground storm sewer pipe directly to the beach (
Phosphate (PO4) concentration was significantly higher at PLA, with up to 15 μM, followed by BAL with 12 μM, and YOL, with nearly 10 μM (
Ammonium (NH3) concentration was just short of significance (p = 0.0568) with slightly higher values at ECO and TRA, with 120 - 125 μm. However, ionized ammonium (
These results suggest that nitrogen concentration seems to be significantly influenced by the trophic condition of groundwater and by groundwater seepage dynamics.
Water quality parameters: (a) Temperature; (b) pH; (c) Salinity; and (d) Conductivity. Mean ± 95% confidence intervals
Water quality parameters: (a) Dissolved oxygen concentration; (b) Turbidity; (c) Chlorophyll-a concentration; and (d) Optical brighteners (OABs) concentration. Mean ± 95% confidence intervals
Dissolved nutrients concentration: (a) Phosphate (PO4); (b) Nitrate (NO3); (c) Nitrite (NO2); (d) Ammonium (NH3); (e) Ionized ammonium (); and (f) Total nitrogen (N). Mean ± 95% confidence intervals
A Principal Component Ordination (PCO) analysis using the entire matrix of water quality parameters showed a strong spatio-temporal water quality gradient that resulted in a significant clustering of sampling sites PLA and BAL which was largely explained by high chlorophyll-a concentration, low conductivity, and in a lesser extent by high PO4 and OABs concentration (
Principal Component Ordination (PCO) of spatio-temporal variation in LBSP across coastal waters
. Three-way permutational analysis of variance (PERMANOVA) of overall water quality parameters
Variable | d.f.* | Pseudo-F | p |
---|---|---|---|
Site | 6173 | 8.44 | <0.0001 |
Date | 8171 | 11.53 | <0.0001 |
Season | 3176 | 14.06 | <0.0001 |
Site × Date | 59,120 | 65.67 | <0.0001 |
Site × Season | 27,152 | 9.45 | <0.0001 |
Date × Season | 8171 | 11.53 | <0.0001 |
Site × Date × Season | 59,120 | 65.67 | <0.0001 |
*Degrees of freedom.
Coral reef benthic communities along the known LBSP stress gradient were showing unequivocal signs of decline, but not all coral reef biological parameters were impacted in a similar fashion. Mean species richness ranged from about 3 to 6 species/transect, depending on the distance from the land-based pollution source and on dominance by Acropora palmata (
Percent living coral cover showed a highly significant increase with increasing distance from LBSP, from values of about 18% in eastern inshore reefs to about 93% across western offshore reef segments (
Green, red and brown macroalgae spatial distribution also followed a non-significant trend of increasing cover in close proximity to LBSP probably as a result of large variability and patchiness across the reef system (
Coral reef benthic community parameters across LBSP stress gradient: (a) Species richness (S); (b) Species diversity index (H’c); (c) Evenness (J’c); and (d) Variation in taxonomic distinctness (sΔ+). Mean ± 95% confidence intervals
Coral reef benthic community parameters across LBSP stress gradient: (a) Percent coral cover (S); (b) Percent Acropora palmata cover; (c) Percent Pseudodiploria clivosa cover; and (d) Percent P. strigosa cover. Mean ± 95% confidence intervals
Coral reef benthic community parameters across LBSP stress gradient: (a) Percent green magraoalgal cover (S); (b) Percent red macroalgal cover; (c) Percent brown macroalgal cover; (d) Percent filamentous algal turf cover; (e) Percent Crustose Coralline Algal (CCA) cover; and (f) Percent cover of Sand, Pavement and Rubble (SPR). Mean ± 95% confidence intervals
are also known to be impacted by significant sediment bedload due to east-west littoral drift and sig- nificant shoreline erosion.
The spatial gradient of reef conditions was evident from regression analyses. There was a highly significant (p = 0.0022) non-linear regression between coral species richness and linear distance from LBSP (
Non-linear correlation between coral parameters and distance from pollution source: (a) Species richness (S); and (b) Variation in taxonomic distinctness (sΔ+)
Linear correlation between coral parameters and distance from pollution source: (a) Percent coral cover; and (b) Percent Acropora palmata cover
(PR-E) was dominated by a sand veneer across the reef surface and brown macroalgae. There was a second cluster of three eastern reefs which were dominated by filamentous algal turfs and opportunistic Pseudodiploria clivosa. A third cluster was composed by a combination of mid and western reefs with moderate to high dominance by Acropora palmata, and a final cluster of mid and western offshore reefs almost exclusively dominated by A. palmata. This PCO analysis showed a solid resolution (80.6%) of the observed spatial variation in benthic community structure, which also resulted statistically significant (
There was also a highly significant correlation between percent cover of A. palmata and water quality parameters such as salinity, and the concentration of dissolved oxygen, OABs, PO4,
Principal Component Ordination (PCO) analysis of spatial variation of coral reef benthic community structure
. Three-way permutational analysis of variance (PERMANOVA) of spatial patterns of variation in benthic com- munity structure
Variable | d.f.* | Pseudo-F | p |
---|---|---|---|
Distance | 2.57 | 19.34 | <0.0001 |
Segment | 1.58 | 3.61 | 0.0157 |
Site | 11.48 | 12.98 | <0.0001 |
Distance × Segment | 5.54 | 14.52 | <0.0001 |
Distance × Site | 11.48 | 12.98 | <0.0001 |
Segment × Site | 11.48 | 12.98 | <0.0001 |
Distance × Segment × Site | 11.48 | 12.98 | <0.0001 |
*Degrees of freedom.
. Significant and marginally significant correlations (Pearson) of selected benthic community parameters and water quality parameters
Sites | A. palmata | P. clivosa | Green macroalgae | Algal turf |
---|---|---|---|---|
Temperature (˚C) | NS* | NS | NS | NS |
Salinity | 0.8918, p = 0.0169 | −0.9882, p = 0.0002 | −0.8140, p = 0.0487 | −0.8193, p = 0.0460 |
Conductivity | 0.7956, p = 0.0584 | −0.9554, p = 0.0029 | NS | −0.8163, p = 0.0475 |
Turbidity | NS | NS | NS | NS |
pH | NS | NS | NS | NS |
Dissolved oxygen | 0.8300, p = 0.0409 | −0.9719, p = 0.0012 | NS | −0.8229, p = 0.0443 |
Chl-a | NS | NS | NS | NS |
OABs | −0.8895, p = 0.0106 | 0.9882, p = 0.0002 | 0.8129, p = 0.0492 | −0.8201, p = 0.0457 |
PO4 | −0.9174, p = 0.0099 | 0.8923, p = 0.0168 | NS | NS |
NH3 | NS | 0.8561, p = 0.0296 | NS | NS |
−0.9084, p = 0.0122 | 0.9857, p = 0.0003 | 0.8204, p = 0.0455 | −0.8102, p = 0.0506 | |
NO3 | −0.8770, p = 0.0218 | 0.9869, p = 0.0003 | 0.8068, p = 0.0524 | −0.8231, p = 0.0442 |
NO2 | −0.9188, p = 0.0096 | 0.9794, p = 0.0006 | 0.8225, p = 0.0445 | −0.7992, p = 0.0565 |
Total N | −0.9291, p = 0.0074 | 0.9431, p = 0.0048 | 0.8120, p = 0.0497 | NS |
There was also a significant correlation between the distribution of filamentous algal turf and salinity, conductivity, and the concentration of dissolved oxygen, OABs,
Coral reefs have significantly declined across an east-west LBSP gradient. Coral species richness and several species diversity indices have declined in proximity to LBSP, are high across moderately disturbed areas, and decline again at remote reef segments far from LBSP disturbance due to dominance by Acropora palmata. This pattern followed the classical intermediate disturbance hypothesis [
Local non-point source sewage pollution sources documented in this study across the Playa Puerto Nuevo area were numerous and included raw sewage spills from sewer pipes that illegally empty at the beach, illegal connections from private properties to storm water sewers, broken sewage pipes by corrosion or beach erosion from a road along the shoreline, overloaded and leaking septic tanks from properties at nearly sea level, and illegal dumping of sewage from septic tank cleaning trucks [
A key concern associated to sewage and eutrophication impacts was the elevated mean chlorophyll-a concentration range found in this study on sites known to be polluted (5 - 25 μg/L), which represented up to 17 - 83 times higher than the recommended concentration for coral reef waters (0.3 - 0.5 μg/L) [
milarly,
Poor water quality pulses are often discrete events in time and space that can become chronic and/or widespread depending on their frequency and severity. In the particular case of BAL in this study, pulse impacts were dramatic as a raw sewage pipe was deliberately opened to free local sewers from Playa Puerto Nuevo community from obstructions and spillovers, but impacts were discrete in time and so were coral mortality pulse events. In the particular case of PLA, raw sewage was chronically mixed with storm waters, emptied just east of the Acropora palmata reef system (
Sewage impacts often result in a combination of system- and species-specific responses, as well as cascading direct and indirect effects that could result in major long-term phase shifts in benthic community structure, favoring dominance by fleshy macroalgae and non-reef building taxa [
A nearly continuous strong east-west LBSP gradient, in combination with high turbidity and sediment bedload smothering corals, has also been documented in the past to affect coral reefs adjacent to the shoreline, with extreme pulse turbidity events reaching local reefs with values as high as 125 NTU [
A final concern is the role of chronic LBSP on potentially magnifying the severity of climate change-related impacts over already stressed out coral reef resources. Coral reefs should be viewed as a coupled social-ecolog- ical system in the context that multiple human activities and social structures can profoundly influence the dy- namics of factors such as human population growth, environmental conditions, and natural resource availability, distribution, and condition. Climate change forecasts suggest increased SST and recurrence of massive coral bleaching events across the wider Caribbean region [
Chronic LBSP leads to increased exposure of coral reefs to cumulative and synergistic stress. This could be affected by the severity, frequency, duration and spatial extent of pulse (discrete), cumulative and synergistic events. Such combined impacts may lead to multiple species-specific threshold responses that still remain largely unknown for most taxa, and may lead to increased sensitivity to environmental- or climate-related stress. Sensitivity could be described as the degree to which any stress level may modify a response of populations to ecosystems. A key example could be the combination of SST above the mean monthly maximum (annual highest SST) for any given locality and the chronic exposure to sediment-laden, nutrient-loaded, sewage-polluted runoff. Higher SST may lead to altered benthic microbial communities, but the combination of high SST + high dissolved nutrient loads may lead to potentially stronger alterations, which may lead to increased states of sensitivity, and eventually to a magnified state of vulnerability.
Under predicted escalating climate change impacts the narrow window still available to protect threatened coral reef resources, such as Elkhorn coral, Acropora palmata, is rapidly being closed by human negligence. Natural resource management has become a major challenge in degraded ecosystems due to the increasing vulnerability to climate change, combined with declining ecological conditions of key resources, and weak adaptive capacity and governance. Losing A. palmata may predispose Caribbean reefs to a dangerous and potentially irreversible loss of resilience in a human time scale [
Chronic LBSP has resulted in a significant decline of extensive stands of threatened Elkhorn coral, A. palmata. Sporadic pulse impacts of nutrient-loaded, turbid and polluted runoff documented in the past [
The most critical corrective management action identified in this study was the imperative need to eliminate illegal raw sewage dumping from septic tank effluents, malfunctioning sewers, and other non-point sources at nearby Puerto Nuevo Public Beach by improving sewer systems and upgrading existing sewage treatment plant facilities. A first step was already taken with the expansion of the sewage pipes system to connect a large portion of the community. Nonetheless, there is still a need to prepare an inventory of septic tanks, their condition, and their potential leakage to saline groundwater on properties located along the shoreline. There is also a need to eliminate illegal connections of private houses to storm sewers and other illegal raw sewage discharges directly to coastal waters. There is a need to improve the implementation of erosion-sedimentation controls on any construction activity across adjacent watersheds or coastal waters. A moratorium in the implementation of existing plans to expand the adjacent rip-rap as a method to control beach erosion is also strongly recommended. Instead, the alternative of using semi-artificial reef technology to reduce or modify wave action and littoral drift should be thoroughly evaluated and implemented to reduce beach erosion, but also to reduce further impacts of turbidity and sediment bedload to adjacent coral reefs.
There is also a need to implement a permanent long-term ecological monitoring program for A. palmata, in combination with a standard water quality monitoring program. Plans are also already underway to expand the existing Community-Based High-Energy Reef Rehabilitation Program led by NGOs Vegabajeños Impulsando Desarrollo Ambiental Sustentable (VIDAS) and Sociedad Ambiente Marino (SAM), in collaboration with the Coral Reef Research Group of the Center for Applied Tropical Ecology and Conservation (CATEC) at the University of Puerto Rico, aimed at propagating A. palmata and reintroducing the species at nearby depleted reefs.
Also, the community-based plan to designate the Vega Baja-Manatí Submarine Gardens Natural Reserve was already submitted for final evaluation by the PPRDNER as a critical strategic tool to manage conflicting uses along the coastal areas of concern that still support significant natural resources, including A. palmata. This should provide an unprecedented opportunity to improve community-based participation in decision-making processes regarding management of the proposed reserve. However, there are critical issues that still need to be addressed, including the implementation of effective pollution controls of storm water runoff from Vega Baja downtown urban areas and from the adjacent landfill. There is also a need to study and model complex local ocean circulation dynamics in order to understand pollutants movement, as well as the connectivity between terrestrial and marine systems. In addition, a strong and continuous community outreach and educational program still needs to be implemented to improve local support for the proposed natural reserve designation, but also as a tool to educate local communities and decision makers regarding the critical importance of the conservation and rehabilitation of local coral reef ecosystems. This could become a major behavior-modifying and community-based engaging tool to foster improved participation through a co-management model.
In the context of forecasted increasing impacts from sea-surface warming trends and oceanic acidification associated to climate change, there is no time to waste to implement immediate actions to protect A. palmata stands and rehabilitate coral reef resilience, ecological functions, benefits and services. Failing to implement rapid and effective solutions may represent an irreparable loss of a significant population of an already severely depleted species through the entire Atlantic. Chronic unsustainable LBSP and lack of governance constitute a major roadblock to the conservation and rehabilitation of coral reefs in face of current and forecasted climate change impacts. The combination of climate-related effects and uncontrolled local anthropogenic stressors would be devastating for these coral reefs and may result in the unprecedented permanent loss of the first line of defense against storm swells and sea-level rise. The price of no action would be too high for a small island with limited economic resources. The conservation and rehabilitation of declining coral reef resources must be one of the top critical priorities for implementing any climate change mitigation and adaptation plan, but roadblocks to conservation need to be eliminated first.
This work was possible thanks to funding provided by the National Science Foundation (HRD #0734826) through the Center for Applied Tropical Ecology and Conservation (CATEC), and the University of Puerto Rico’s Central Administration to E.A. Hernández-Delgado. Our appreciation for the logistical field support provided by Ricardo Laureano (Vegabajeños Impulsando Desarrollo Ambiental Sustentable—VIDAS), and to Jaime Fonseca and Alex Mercado (Department of Biology, University of Puerto Rico, Río Piedras Campus) for laboratory and logistical support. Our thanks also to volunteer members of NGO Sociedad Ambiente Marino (SAM) and its Students Chapter (CESAM) for their support. This publication was part of the B.Sc. Honors Thesis project of G. Díaz-Ortega and a contribution from CATEC’s Coral Reef Research Group and SAM’s collaborative Coral Reefs Conservation and Rehabilitation Project.