Large-scale coral recruitment patterns on Mona Island, Puerto Rico: evidence of a transitional community trajectory after massive coral bleaching and mortality
Patrones a gran escala del reclutamiento de coral en Isla Mona, Puerto Rico: evidencia de una trayectoria transitoria de comunidad después del blanqueamiento y mortalidad coralino masivo
Edwin A. Hernández-Delgado1*,2*, Carmen M. González-Ramos1,2,3* ]]>
2
Abstract
Coral reefs have ]]>
Orbicella annularis species complex) which show no apparent signs of recovery through larval sexual recruitment. We addressed coral recruit densities across three spur and groove reef locations along the western shelf of remote Mona Island, Puerto Rico: ]]>
2 at LCS, 4.5 to 9.5/m2 ]]>
O. annularis species complex was limited or non-existent. The lack of recovery could be the combined result of several mechanisms involving climate change, YBD disease, macroalgae, fishing, urchins and Mona Island’s reefs limited connectivity to other reef systems. There is ]]>
D. antillarum. Failing to recognize the importance of ecosystem-based management and resilience rehabilitation may deem remote coral reefs recovery unlikely.
Key words: Climate change, coral decline, coral recruitment, community trajectory, Mona Island, Puerto ]]>
Resumen
Los arrecifes de coral han disminuido en gran medida en el noreste del Caribe después de los ]]>
Orbicella annularisOrbicella annularis) que no muestran signos evidentes de recuperación a través del reclutamiento larval sexual. Nos centramos en las densidades de coral recluta en tres sitios de coral espuela y surco a lo largo de la plataforma occidental de la remota Isla de Mona, Puerto Rico: Punta Capitán (PCA), Pasa de Las Carmelitas (PLC) y Las Carmelitas-Sur (LCS). Los datos fueron recolectados durante noviembre de 2012 a lo largo de 93 transectos a través de tres zonas de profundidad (<5m, 5-10m, 10-15m). Se documentaron un total de 32 especies de corales (9 octocorales, 1 hidrocoral, 22 scleractinios) entre la ]]>
m2 en el PCA, 6.3 y 7.2/m2 en LCS, 4.5 a 9.5/m2 en el PLC. Diferencias ]]>
O. annularis
del complejo de especies fue muy limitado e incluso inexistente a través de zonas extensas de arrecife. La falta de recuperación puede ser el resultado combinado de varios mecanismos que implican cambio climático, brotes crónicos de YBD, macroalgas, pesca, erizos y conectividad limitada de los arrecifes de la isla Mona a otros sistemas de arrecife. También hay una necesidad de impulsar la rehabilitación de la estructura trófica de peces, con énfasis en la recuperación de gremios herbívoros y las poblaciones agotadas de D. antillarum. Al no reconocer la importancia de la gestión de rehabilitación y capacidad de recuperación basado en los ecosistemas se estima que la recuperación de arrecifes de coral es muy improbable.
Palabras clave: Cambio ]]>
Coral larval recruitment is critical for the maintenance of reef biodiversity, ecosystem resilience and benthic community recovery after disturbances across multiple spatial scales (Gittings, Bright, Choi & Barnett, 1988; Sammarco, ]]>
Diadema antillarum (Phillipi 1845) (Lessios, 1988; Gardner et al., 2003), with paramount long-term impacts in adult coral assemblages and in the ]]>
Juvenile coral depth distribution often follows the distribution of adult parental colonies (Bak & Engel, 1979; Harriott, 1985). But Caribbean-wide coral reef decline has been characterized by significant losses in percent live tissue cover ]]>
Orbicella (=Montastraea) annularis species complex (Ellis ]]>
O. faveolata (Ellis & Solander, 1786) (Weil, Cróquer & Urreiztieta, 2009), and caused a rapid decline within the O. annularis species complex in Mona Island (Bruckner & Bruckner, 2006; Bruckner & Hill, 2009). These factors led to massive coral recruitment failure of multiple species, resulting in a major decline in the natural recovery ability of critical reef-building species such as O. annularis (Edmunds & Elahi, 2007; Hernández-Pacheco, Hernández-Delgado, ]]>
Successful coral recruitment is critical for sustaining slow-growing, low-recruiting massive coral species (Harrison & Wallace, 1990; Szmant, 1991). But several long-term studies have shown very limited sexual recruitment success ]]>
O. annularis species complex (Rogers et al., 1984; Edmunds & Elahi, 2007; Irizarry-Soto & Weil, 2009), even at Mona Island (Bruckner & Hill, 2009). Edmunds (2004) also found a positive correlation between juvenile coral density and mean sea surface temperature (SST), with slower growth and higher mortality under high SST, in a pattern leading to changes in relative generic abundance. ]]>
Climate change has become one of the most significant and imminent threats to coral reefs at a global scale (Hoegh-Guldberg, 1999; Buddemeier et al., 2008). Recent modeling efforts have suggested that current trends in sea surface warming, increasing atmospheric CO2 concentration, and OA might have paramount negative consequences on coral reef ecosystems and their services (Buddemeier et al., 2008; 2010), as well as in the overall marine ]]>
Even remote coral reefs have undergone significant recent decline as a result of regional climate change-related impacts (Goreau, Hayes & McClanahan, 2000; McClanahan & Muthiga. 1998; McClanahan, 2000; Walther et al., 2002) and have showed limited recovery ability (Gardner et al., 2005; Sandin et al., 2008; Birkeland et al., 2013). Coral reef recovery on remote habitats depends on the functional redundancy of impacted coral ]]>
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Materials and Methods
Study sites: This study was carried out in November 2012 across three spur and groove fringing reef locations along the western shelf of Mona Island, Puerto Rico: Punta Capitán (PCA, 18°06.283’N, 67°56.137’W), Pasa de Las ]]>
Coral recruit density: Data was ]]>
m2) photoquadrat fixed to the camera housing. Any coral colony <5cm was treated as a coral recruit. Coral species with sexually mature small sizes, such as Siderastrea radians (Pallas, 1766), were also included in the counts as they were largely abundant across study sites. Efforts were made to avoid sampling areas with high sediment ]]>
Statistical analyses: A two-way multivariate analysis of similarity (ANOSIM) was used to test the null hypothesis of no significant difference in coral recruit density, ]]>
Results
A total of 347 coral recruit colonies of 32 coral species (9 octocorals, 1 hydrocoral, 22 ]]>
Table 1). This included 17 species at PCA subdivided in 3 species across the shallow reef segment, 11 species across the middle depth segment, and 13 across the deeper segment. There were also 15 species at LCS subdivided in 8 species across shallow, 7 across the middle, and 10 across the deeper segment. A total of 18 species of coral recruits were observed at PLC, with 9 species across the shallow, 8 across the middle, and 16 across the deeper zone. Coral recruit community structure was significantly different among locations ]]>
p=0.0260), particularly between PCA and LCS (p=0.0060), but not among depth zones (Table 2). There was a significant site x depth interaction (p=0.0160). Coral recruit assemblages were overall dominated by ]]>
Siderastrea radians (Pallas 1766) and mustard hill coral Porites astreoides (Pallas 1766), representing 33% and 31% of the total coral recruit colony abundance. These were followed by lettuce coral Agaricia agaricites (Linnaeus 1767), brain coral Diploria strigosa (Dana 1846), and finger coral Porites porites (Pallas 1766), ]]>
Fig. 1).
Shallow reef zone abundance of S. radians reached 3.7 and 3.4colonies/m2 at PLC and LCS, respectively. Abundance of P. ]]>
reached 2.9 and 2.2colonies/m2 at PLC and LCS, respectively. Middle reef zone abundance of Abundance of P. astreoides reached 2.7 and 2.0colonies/m2
at PCA and PLC, respectively. S. radians reached 2.5colonies/m2 at LCS. P. astreoides
m2. Siderastrea radians was dominant at the deeper zone of LCS with 2.5colonies/m2. These corals were largely growing on formerly O. annularis species complex dominated habitats. Most of the dominant reef-building corals across these habitats died following the 2005 massive coral bleaching event. Nonetheless, recruits members of the O. annularis species complex were very rare across the shelf, and were ]]>
O. annularis (2%) and 3 of O. faveolata (0.9%) were documented out of the 347 recruit colonies found across the 465 surveyed quadrats, suggesting that natural population recovery seven ]]>
Total coral recruit density was significantly different among sites (p=0.0020), but not among depth ]]>
Fig. 2a). The highest overall densities were documented at the deeper zones of PCA and LCS, with 10.5colonies/m2 and 7.2colonies/m2, respectively. The highest density of the middle depth zone was observed at PCA with 6.4colonies/m2
, while the highest density of shallower zones was observed at LCS with 9.6colonies/m2. Coral species richness was significantly different among sites (p=0.0130), particularly between PCA and LCS (p=0.0070), and between PCA ]]>
p=0.0130) (Fig. 2b). No significant difference among depth zones was observed. The highest species richness was at deeper zones of PCA (2.9/transect), PLC (2.6/transect), and LCS (2.2/transect). H’n was significantly different among sites (p=0.0420), particularly ]]>
p=0.0320) (Fig. 2c). The highest H’n was documented at deeper zones of PCA (0.8912) and PLC (0.7385), followed by the shallow zone of PLC (0.7385). J’n was significantly different between shallow and deep zones (
p=0.0310) (Fig. 2d). No site-specific effects were observed. The highest J’n was observed at the deeper zones of PLC (0.7281), PCA (0.6830), and LCS (0.6725).
Percent macrocalgal ]]>
Fig. 3). Most macroalgae were Phaeophytes dominated by Dictyota spp. and Lobophora variegata Lamouroux 1817. There was a highly significant non-linear negative correlation (r2=0.6864, p<0.0001) between increasing percent ]]>
Fig. 4). PCO analysis showed four general clustering patterns of coral reef bottoms, with one cluster largely dominated by P. astreoides recruits, and in a lesser degree by Montastraea cavernosa Linnaeus 1767, and Agaricia ]]>
Fig. 5). A second cluster was determined by abundant S. radians recruits, followed by A. agaricites and
D. strigosa. A third cluster was dominated by P. astreoides. A final cluster was dominated by open reef bottoms largely devoid of corals, and dominated by brown macroalgal overgrowth.
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Discussion
Coral recruit communities at remote Mona Island showed low densities and dominance by short-lived brooder coral species seven years after the 2005-2006 massive bleaching event and the subsequent post-bleaching mass coral mortality. Differences in coral recruit community structure can be attributed to slight variation ]]>
O. annularis species complex was very limited and even non-existent across extensive reef zones. Instead, dead coral surfaces were largely overgrown by unpalatable brown macroalgae
L. variegata and Dictyota spp. Red encrusting algae Peysonnellia spp. were also abundant. Mona’s isolated reef systems have followed a transitional trajectory leading to a major phase shift favoring macroalgae and non-reef building, ephemeral coral taxa. Lack of coral reef recovery following major disturbances, including climate change, has been a concerning ]]>
D. antillarum population recovery, altered microbial communities associated with crustose coralline algae (CCA) that may negatively affect coral larval settlement cues, and Mona Island’s reefs limited connectivity to other reef systems which highly limits potential successful larval recruitment from other locations. ]]>
The observed trend of low coral recruit densities and dominance by short-lived brooder coral species is very similar to recent observations from other Caribbean reefs where massive reef-building species have largely declined and have shown limited or no net recovery (Rogers & Miller, 2006; Miller et al., 2009; Hernández-Pacheco et al., 2011; Edmunds, 2013), which suggest a long-term coral recruitment decline across the region. Mean coral recruit density ranged from 1.2 to 10.5/m2 at PCA, 6.3 to 7.2/m2 at LCS, 4.5 to 9.5/m2 at PLC in our study. But earlier studies across the wider Caribbean showed higher recruit density values than most recent accounts. Bak and Engel (1979) documented coral recruit ]]>
m2 across the 3-9m depth zone, and of 12.9/m2 across the 9-17m depth zone at Curaçao. Rogers et al. (1984) found coral recruit densities ranging from 13 to 42colonies/m2 at Salt River Canyon, St. Croix, USVI across depth ranges similar to this study. ]]>
m2 at Belize, 26.7/m2 at St. Croix, 28.9/m2 at Barbados, 26.6/m2 at Port Antonio, 15.6/
m2 at Bonaire, and 33.8/m2 at Grenada. They also found that highest coral recruit densities correlated with high densities of D. antillarum and lower percent algal cover. Tomascik (1991) documented relatively common recruits of O. annularis, Siderastrea siderea (Ellis & Solander, 1786), and Diploria spp. on settlement plates from non-polluted reefs at Barbados. Bak and Meesters (1999) also found relatively common juvenile colonies of O. annularis species complex, S. siderea, and other massive coral species at ]]>
m2 within a no-take marine protected area (MPA), and from 4.5 to 6/m2 across non-MPA sites at Exuma Cays, Bahamas. But large massive Caribbean-wide disturbances, such as recurrent massive bleaching events ]]>
D. antillarum (Lessios, 1988) have resulted in a major transition in the ecological state of coral reefs. A key characteristic of such a change has included rapidly declining coral recruit densities.
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Recent studies have documented declining coral recruit densities across the Caribbean. Irizarry-Soto and Weil (2009) found a decline from 4.8 to 2.8 coral recruit colonies/m2 between 2003 and 2005, and very low recruit abundance of massive reef-building species in La Parguera, Puerto Rico. Coral recruit density within a no-take MPA in Exuma Cays, Bahamas, increased ]]>
m2 for P. astreoides, 1.4/m2 for A. agaricites, and 2.1/m2 for O. annularis in 2004 to 8.4/m2, 2.3/m2, and 3.1/m2 in ]]>
m2 in 2004 to 3.5/m2 in 2007 for P. astreoides. Densities of 0.6/m2 for A. agaricites and 2.2/m2 for O. annularis in 2004 showed no ]]>
O. annularis and O. faveolata due to YBD outbreaks (Bruckner & Bruckner, 2006), failed recruitment, minimal ]]>
O. annularis species complex across the same surveyed sites in this study were either killed or are showing partial mortality due to YBD infections (Hernández-Delgado, unpublished).
Rapidly declining coral recruitment and lack of coralline community recovery across the Caribbean significantly contrasts recovery trends documented in isolated coral reefs off Western Australia where coral cover increased from 9 to 44% within 12 years of the 1998 massive coral bleaching event by a combination of coral tissue regeneration of remnant surviving colonies and coral recruitment (Gilmour et al., 2013). Diaz-Pulido et al. (2009) ]]>
L. variegata, a natural seasonal decline in macroalgal dominance, and an effective MPA system. However, the benefits from MPAs may not be great enough to offset the magnitude of losses from acute thermal stress events (Hughes et al., 2011; Selig, ]]>
We argue that shifting benthic community trajectories have largely impacted coral recruitment dynamics. The observed shift in coral recruit biodiversity is a consequence of the massive post-bleaching coral mortality in 2005-2006 ]]>
O. faveolata. Significant physiological fragmentation in O. annularis and O. faveolata
colonies from Culebra Island, Puerto Rico, resulted in permanently halting sexual reproduction in fragmented remnants since the 2005 bleaching episode (Hernández-Delgado, unpublished), similarly to declining reproduction in coral physiological fragmentation experiments documented elsewhere (Szmant-Froelich, 1985; Szmant, 1986; 1991; Szmant & Gassman, 1990; Soong 1993). There is also evidence from the eastern Pacific that most of the recruitment following a massive bleaching and mortality event occurs largely due to rapid recruitment of ephemeral, high-recruiting coral taxa which can be ]]>
O. annularis (Hernández-Pacheco ]]>
We also argue that shifting herbivory dynamics, in combination with natural eutrophication pulses, may indirectly affect coral recruitment dynamics due to algal out-competition of corals. Severely depleted
D. antillarum populations, as well as low abundance of large sized fish herbivores (Scaridae), across the Mona Island shelf (Hernández-Delgado unpublished), and grazing preferences of remnant grazer guilds (Szmant, 2002) is probably associated to the significant shift in dominance by L. variegata and Dyctiota spp., which in turn are significantly affecting ]]>
L. variegata and Dictyota spp. (Box & Mumby, ]]>
Ramicrusta spp. (Eckrich & Engel, 2013) can strongly out-compete juvenile corals due to shading and abrasive effects, or inhibit successful coral larval recruitment. Kuffner et al. (2006) also found experimental evidence that the combined presence of intermingled unpalatable brown macroalgae and cyanobacteria caused either recruitment inhibition, avoidance behavior or larval mortality in multiple coral species. Further, we propose that natural nutrient enrichment pulses can fuel up algal growth. Physical meso-scale oceanographic processes such as internal waves or seiches (Wolanski ]]>
Hughes and Connell (1999) found that coral reef assemblages that are similar in coral community composition, but under different management regimes may show profound differences in recruitment dynamics and species turnover, with major ]]>
D. antillarum and fish herbivore guilds seem to have a significant role in fostering increased coral recruitment rates. According to Mumby et al. (2007), coral recruit density can increase up to 2-fold within no take MPAs as a result of reduced fishing pressure and weak predator–prey interactions that can create trophic cascades that increase the ]]>
D. antillarum is occurring at both local and regional scales, and that urchin grazing is creating conditions favoring coral recruitment. Nonetheless, D. ]]>
recovery in Puerto Rico has been patchy and spatially limited even three decades after mass mortality (Ruiz-Ramos, Hernández-Delgado et al., 2011). Long-term trends documented in Mona Island and elsewhere around Puerto Rico have also shown that brown macroalgae have become the dominant component of many coral reefs (Hernández-Delgado, 2005; Ballantine et al., 2008; García-Sais et al., 2008). If macroalgae dominate open available substrates, they might permanently inhibit coral recruitment either due ]]>
]]>
Natural recovery of remote coral reefs may seem increasingly difficult due to regional scale of ecosystem decline across the Caribbean which compromise natural connectivity to other reefs Lack of coral reef recovery also implies declining coral functional redundancy and coral reef ecosystem resilience, which could in turn result in a long-term decline in ecological scales of connectivity. Coral reefs at Mona Island are high-circulation, oligotrophic, oceanic reef systems, located far from known anthropogenic pollution sources, but also far from potential ]]>
Replenishment of depleted coral engineer species will require immediate novel efforts (i.e., low-tech coral farming) to rehabilitate their populations. It will also require large-scale, ecosystem-based management of reef fisheries to foster the ]]>
D. antillarumD. antillarum populations should be implemented across shelf-wide scales. These will represent important steps towards ]]>
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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 of the University of Puerto Rico (UPR). We also acknowledge support provided by UPR Department of Biology and by ]]>
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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, edwin.hernandezdelgado@gmail.com, carmenbiology@hotmail.com;
2. Sociedad Ambiente Marino, PO Box 22158, San Juan, PR 00931-2158, drakho76@gmail.com
3. University of Puerto Rico, Department of Biology, PO Box 23360, San Juan, PR 00931-3360, carmenbiology@hotmail.com ]]>
Received 01-IX-2013 Corrected 31-IV-2014 Accepted 01-IV-2014 ]]>20112008200625441-4502003252289-293197954341-35219993956-652008I375-4062005141377-13902006511969-1981201363967-9742007342139-14920066967-7320098719-3120086395-41120101093-43-4375-39720069271-28020012199716S101-S113199767461-488200485197197201-20220098733-432009444e5239201215338-346201051111e1396920133281-842004269111-1192007773-182005436686-68820101069-83200875-1162003301958-960200586174-184201334069-7119882225-230200726319-332199224199754327-3582000141-1819852181-881990133-2072005281-35620112111-13199950839-86620073181737-174219942651547-1551198711339-59199944932-9402000812250-2263201130653-660200945269-2812006323107-117201381212e825792002199010289-307199816683-97198819371-393200625186200968158-1622007200040587-597199825122-130200119400-4172005862055-20602005311-7201441-152006200928925-937199919027-3520071048362-83672010511e86572001223121-13120091977590-595196613131-144201220920132013.1984369-762006306103-114201187113-127199136496-5142008322e15482012181561-1570194819821557-6619931277-8319854295-3001986543-5419917413-25200225743-76619908217-224199177262-2692009581428-143620079840-502002416389-39520115759-770200435-68200983195-20820098745-5519981281-118199515357-36820082763-72