Us Caribbean Marine Managed Areas Data Report

US CARIBBEAN MARINE MANAGED AREAS DATA REPORT

Prepared by

Diana Beltran University of Rhode Island, Kingston 02881

Abbreviations and Acronyms Used

ALS Abrir La Sierra BS Bajo de Sico CCRI Caribbean Coral Reef Institute CFMC Caribbean Fisheries Marine Council EEZ Exclusive Economic Zone EFH Essential Fish Habitat FMU Fishing Management Unit FSA Fish Aggregation Area GB Grammanik Bank LB Lang Bank (Red Hind Spawning Aggregation Area) MCD Hind Bank Marine Conservation District MMAs Marine Managed Areas MCE Mesophotic Coral Ecosystems MSFC & M ActMagnuson-Stevens Fishery & Conservation Act MSSA Mutton Snapper Spawning Aggregation NMFS National Marine Fisheries Service NOAA National Oceanographic and Atmospheric Agency NTZ No-take-zone PMA Protected Marine Area PR Puerto Rico PRCRMP Puerto Rico Coral Reef Monitoring Program PR-DNER Puerto Rico-Department of Natural and Environmental Resources TB Tourmaline Bank TCRMP Territorial Coral Reef Monitoring Program USVI United States Virgin Islands VI-DPNR US Virgin Islands Department of Planning and Natural Resources

1. Introduction The oceans have degraded in the last decades as a result of human activities (Mora 2008). This decline is most notorious in coastal areas such coral reefs, where coral cover has decreased more than 50 % worldwide (Gardner 2003; De’ath et al. 2012; Jackson et al. 2014), and species commonly seen in the seventies are rarely observed today, especially commercial reef fishes (Steneck et al. 2009). Conservation efforts are urgently needed to reduce such loss, recover depleted populations and restore natural habitats.

A popular measure to restore natural habitats and populations are Marine Managed Areas or Marine Protected Areas (MPAs). The most restrictive form of an MPA is a no-take zone, defined by a fishing-free geographical space that can restore populations when properly implemented and managed. MMA or MPA act by protecting and increasing the population spawning potential of overexploited species (Roberts 1997). MMAs or MPAs as conservation initiatives are based on the idea that most marine populations are genetically and ecologically connected over hundreds of kilometers by dispersing planktonic larvae. Larval dispersal determines the degree of connectivity among marine populations, providing information on the ideal reserve size to achieve self-recruitment and the minimum spacing among reserves to maintain connectivity and diversity (Sale, 2005). While most marine reserves should work theoretically, it is still uncertain their effectiveness and whether they work as well-connected networks. It is also unknown if MMAs or MPAs count with the necessary information to work as planned and successfully over time.

Figure 1. Puerto Rico Marine Managed Areas. Many factors impact the MMA or MPA's effectiveness to protect marine life, including the degree to which extractive marine activities are restricted or prohibited, size, location, habitat representation, ecological and

genetic connectivity. Usually, the MMA or MPA's positive conservation outcomes are primarily dependent on their stage of establishment and vary from fully protected no-take areas to less protected areas that allow many types of resource extractions or other human disturbances. Also, the level of commitment to managing them varies from highly intervened areas, where habitat restoration happens to areas where only a single study has been done, and no data on their current state exists.

Figure 2. US Virgin Islands Marine Managed Areas.

In the US Caribbean, there are 58 areas with some level of protection, from little protection to permanent no-take zones (Figures 1 and 2). These protected areas range across the five IUCN categories (Ia, II, III, IV, and V) and even include seasonal closures, which under the IUCN definitions are not considered protected areas (Fig. 3). The great majority of these protected areas are in IUCN category IV. Category VI aims to protect, maintain, conserve and restore habitats within the protected areas and needs active management interventions to address the requirements of a particular species or habitats (IUCN 2020). Ideally, the US Caribbean protected areas should reach IUCN category Ia, which are protected areas with full enforcement of the activities within those areas and where human visitation and use is fully controlled and limited. This level of protection ensures the maintenance of habitats and the value of the resources within the areas. These Ia areas, in principle, approximate or equate to no-take areas.

Figure 3. Protected areas in the US Caribbean under the different IUCN designations and including no-take zones.

A key aspect that we have addressed during this report is whether the US Caribbean is on par with the 2030 United Nations goal of 30% of the ocean waters fully protected (CBD/WG2020). If we consider all US Caribbean EEZ waters, only 2.1% presents some form of protection (Table 1). However, if we include only the territorial waters, the protection increases to 29.2% for Puerto Rico and 27.7% for US Virgin Islands (Table 1). This figure includes all Marine Managed Areas, Marine Reserves, National monuments, National Parks, and Fishery Closure Areas in the US Caribbean. If we only consider no-take zones (including seasonal closures) –which are fully protected and in syntony with the UN mandate– the US Caribbean has 0.85% across the entire EEZ. The percentage of no-take zones within the territorial waters of Puerto Rico is 0.94% and 0.03% in the PR EEZ. The percentage of no-take zones within the territorial waters of the USVI is 11.2% and 0.15% in the USVI EEZ (Table 1). These estimates suggest that the amount of area currently under complete protection (i.e., no-take) is far from reaching the 30% UN 2030 goal.

Table 1. Percentage of protected areas in the US Caribbean, including no-take zones and the IUCN categories.

Number of US Caribbean US CARIBBEAN Area (km2) Areas Basin (%) All protected areas (58 MMAs) 4446.25 58 2.1 Ia 125.03 8 0.06 Unassigned 806.58 24 0.38 IV 3264.65 22 1.55 II 63 2 0.03 III 51 1 0.02 V 149 1 0.07 No Take areas (includes seasonal no-take) 1805.12 12 0.85

Number of Territorial Puerto Rico Area (km2) PR EEZ (%) Areas Waters (%) Total Area MMAs : 44 Total 3995.23 44 29.72 Ia 48 6 0.36 Unassigned 693.58 17 5.16

IV 3253.65 21 24.2 No Take in territorial waters (in 9NM) 126.85 5 0.94 No Take EEZ (out 9 NM)* 60.99 3 0.03

Number of Territorial US Virgin Islands Area (km2) USVI EEZ (%) Areas Waters (%) Total Area MMAs : 15 Total 393.03 12 27.68 Ia 77.03 2 5.42 Unassigned 42 4 2.96 IV 11 2 0.77 II 63 2 4.44 III 51 1 3.59 V 149 1 10.49 No Take in territorial waters (in 3 NM) 159.03 5 11.2 No Take EEZ (out 3 NM)* 58 3 0.15

Area PR Territorial Waters (9 NM) (km2) 13443 Area USVI Territorial Waters (3 NM) (km2) 1420 USVI EEZ (km2) 38275 PR EEZ (km2) 182882 Total Area EEZ (km2) 211242 *Note that these MMAs are seasonal, and do not fully meet the IUCN categorization.

While the analysis above was carried out for all protected areas, this report highlights the information available for seven MMAs in the US Caribbean under the vigilance of the CFMC (Aguilar-Perera et al., 2006) with emphasis on the available data, state of the benthic habitats and recommendations to enhance the conservation strategies of these marine resources. The Marine Managed Areas are:

1. Abril la Sierra 2. Tourmaline Bank 3. Bajo de Sico 4. Grammanik Bank 5. Hind Bank Marine Conservation District 6. Red Hind Closure at Lang Bank 7. The Mutton Snapper Closure

For each of the Marine Managed Areas, we provide details about:

● History and description of each Marine Managed Area ● What are the ecosystems present in each Marine Managed Area? ● What are the reported species within each Marine Managed Area? With particular emphasis on commercially important species. ● What is the condition and ecological change through time within each Marine Managed Area? ● The primary scientific studies that have or are taking place within each Marine Managed Area and the significant findings in those studies. ● Which gaps in knowledge exist, and what studies/actions are needed to ensure the long-term sustainability of the Marine Managed Areas? What are the best approaches to address these scientific gaps?

2. Abrir La Sierra (ALS)

2.1 History and description of ALS Abrir la Sierra (Seasonal Fishing Closure Area) is a shelf-edge reef within the EEZ with a total area of 29.5 km2, located 23.5 km west off Punta Guaniquilla, Cabo Rojo, on the western border of the Puerto Rican insular shelf (García-Sais et al. 2010) (Fig 4). The no-take area within ALS is also 29.5 km2 and was established by NMFS via the MSFC & M Act in 1996 to improve fisheries management, emphasizing protecting spawning aggregations of red hind (Epinephelus guttatus) by prohibiting fishing in these areas during the spawning season (Federal Register 1996). ALS is governed by the Caribbean Fisheries Management Council (CFMC), The National Oceanographic and Atmospheric Agency (NOAA), and the Puerto Rico Department of Natural and Environmental Resources (PR-DNER). ALS is a seasonal no-take zone with a closure between December 1 to February 28 (Pittman et al., 2014, Schärer-Umpierre et al. 2014). a b

Figure 4. a. Location of Abrir la Sierra (Seasonal Fishing Closure Area) with extension and location of each of the different habitats. b. ALS benthic habitat categories.

2.2 Marine ecosystems present in ALS The insular shelf that leads to ALS is an extensive platform of pavement, sand, and coral reef habitats that stands as the most extensive continuous neritic terrace of the Puerto Rican insular shelf. The main geomorphological features and habitats present at ALS between 30 and 50 m depth are two internal slope walls, a deep outer shelf terrace, and an insular slope wall. Mesophotic benthic habitats within these reef zones include colonized pavement (hard bottom), rhodolith reefs, a small coral reef, and a primarily unconsolidated habitat of scattered rhodoliths and sand (Figure 4). Inner walls of the deep terrace show

moderate live coral cover, consistent with a coral reef habitat down to a maximum depth of approximately 27 - 28 m. The reef substrate below 30 m consisted mainly of pavement colonized by algae, sponges, and scattered corals that declined in abundance and diversity with increasing depth. Boulder star coral, Orbicella annularis (formerly Montastraea annularis), was the main structural component of the coral reef habitat and was observed to be in good condition (García-Sais et al. 2010).

2.3 Condition and changes through time of marine ecosystems in ALS García-Sais et al. (2010) characterized the closure, and the description is presented below. The benthic ecosystems present at ALS have not been studied again, and thus there is no information available on its current condition.

2.4 Reported species within ALS The mesophotic habitats present at ALS have 84 species/taxonomic groups of benthic algae, sponge, scleractinian corals, hydrocorals, and octocorals (Table 2). The most abundant benthic species/taxonomic groups are algal turfs and the macroalgae Lobophora variegata; among the scleractinian corals, the most representative species is Orbicella annularis (formerly Montastraea annularis) and Agaricia agaricites.

Table 2. Representative benthic species recorded at Abrir la Sierra. Species/Groups Type Species/Groups Type Agaricia agaricites Scleractinian Siderastrea siderea Scleractinian Agaricia lamarcki Scleractinian Stephanocoenia intercepta Scleractinian Eusmilia fastigiata Scleractinian Millepora alcicornis Hydrocoral Helioseris cucullata @ Scleractinian Stylster roseus Hydrocoral Isophyllia sinuosa Scleractinian Iciligorgia schrammi Octocoral Isophyllastrea rigida Scleractinian Pseudopterigorgia sp. Octocoral Madracis decactis Scleractinian Agelas clathrodes Sponge Meandrina meandrites Scleractinian Agelas conifera Sponge Montastraea cavernosa Scleractinian Xestospongia muta Sponge Orbicella annularis @ Scleractinian Lobophora variegata Macroalgae Porites astreoides Scleractinian Dictyota spp. Macroalgae Porites porites Scleractinian Turf algae Turf Scolymia cubensis Scleractinian Filamentous cyanobacteria Cyanobacteria Siderastrea radians Scleractinian @ Shows the valid and updated name of the species, data modified from García-Sais et al. (2010)

The fish community at ALS is composed of 110 species (Tables 3 and 4). Table 3 shows the commercially important fish species found at this site with their fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005), conservation status according to the IUCN red list, and trophic group according to Ennis et al. (2019). In the case of CFMC’s FMU, only those categories that include the largest or most important fish from the commercial point of view have been included in this table. The commercially important species registered at ALS are groupers (red hind, Nassau, yellowfin grouper, coney, graysby) and snappers (schoolmaster, mutton snapper, dog snapper, cubera snapper). Table 4 shows representative fish species found at this site and their fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005). It

should be noted that in 2010, the presence of the lionfish was already registered in this Marine Managed Area.

Table 3 Commercially important fish species found at ALS. Scientific Name Common Name Fisheries2 UICN Red List Trophic Status3 Group1 Epinephelus guttatus Red hind Groupers Least Concern Invertivore Mycteroperca venenosa Yellowfin grouper Groupers Near Threatened Piscivore Cephalopholis fulva Coney Groupers Least Concern Piscivore Cephalopholis cruentata Graysby Groupers Least Concern Piscivore Lutjanus cyanopterus Cubera snapper Snappers Vulnerable Piscivore Lutjanus analis Mutton snapper Snappers Least Concern Piscivore Lutjanus apodus Schoolmaster Snappers Least Concern Piscivore Lutjanus jocu Dog snapper Snappers Data Deficient Piscivore Ocyurus chrysurus Yellowtail snapper Snappers Data Deficient Planktivore Caranx crysos Blue runner Jacks Least Concern Piscivore Calamus pennatula Pluma porgy Porgies Least Concern Invertivore Balistes vetula Queen trigger Triggerfish Near Threatened Invertivore Pomacanthus arcuatus Gray angel Angelfish Least Concern Spongivore Holacanthus ciliaris Queen angel Angelfish Least Concern Spongivore Sparisoma aurofrenatum Redband parrotfish Parrotfishes Least Concern Herbivore Sparisoma viride Stoplight parrotfish Parrotfishes Least Concern Herbivore 1 Modified From Ennis et al. 2019; 2 According to CFMC 2005; 3 According to UICN Red List Status; fish names from Garcia- Sais et al. 2010, 2012.

2.6 Primary scientific studies that have or are taking place within ALS The scientific studies that have been conducted in ALS are related to developing new methodologies to understand the spawning aggregation of the red hind. The most recent studies carried out at ALS, and their main findings are summarized below.

Rowell et al. (2011) used passive acoustics to map a spawning aggregation of the red hind (Epinephelus guttatus). The study was conducted during January and February 2010 on days and hours known to have high call rates. A hydrophone attached to a mobile digital audio recorder was deployed from a boat. The vessel drifted over a suspected spawning aggregation area while the global positioning system (GPS) coordinates were simultaneously recorded. After evaluating audio recordings, occurrences and intensities of red hind calls were charted with their GPS locations in GIS. The eastern and western boundaries of the aggregation were successfully mapped. Divers confirmed the presence of reproductively active individuals. These time-saving methods and technologies can be expanded to other soniferous groupers and potentially can be automated so that results can be determined in near-real-time.

Rowell et al. (2012) used passive acoustic and diver-based underwater visual census (UVC) to develop an efficient method for estimating red hind density from sound production at spawning aggregations. Red hind sound production was recorded from November 2010 to April 2011. UVC surveys were conducted during the spawning season to assess changes in red hind density over a fixed time and area. Sound recorded from

18:00 to 19:00 h was representative of total daily changes in red hind sound production and was selected to develop an efficient density estimation model. Pronounced daily changes in sound production and density were observed after the December 2010 and January 2011 full moons. Two hourly sound level measurements were compared to densities estimated by UVC surveys, yielding significant linear regressions, which were used to predict changes in fish density as measured at the aggregation site. Passive acoustic methods allowed them to predict changes in red hind density and habitat use at a higher temporal resolution than previously possible with traditional methods. Red hind sound production and inferred densities can be monitored and analyzed efficiently for multiple aggregation sites simultaneously, documenting short-term and long-term changes in red hind densities at spawning aggregation sites and providing information to develop management strategies.

Table 4. Other fish species recorded at ALS. Scientific Name Common Name Fisheries1 Calamus calamus Saucereye porgy Porgies Scomberomorus regalis Cero - Pseudupeneus maculatus Spotted goatfish Goatfish Mulloidichthys martinicus Yellow goatfish Goatfish Haemulon flavolineatum French grunt Grunts Haemulon plumierii White grunt Grunts Haemulon sciurus Bluestriped grunt Grunts Lachnolaimus maximus hogfish Wrasse Holocentrus rufus Longspine squirrelfish Squirrellfish Holocentrus adscensionis Squirrelfish Squirrellfish Myripristis jacobus Blackbar soldierfish Squirrellfish Melichthys niger Black durgon Triggerfish Bodianus rufus Spanish hogfish Wrasses Sphyraena barracuda Great barracuda - Pterois volitans Lionfish - Ginglymostoma cirratum Nurse shark - Carcharhinus perezi Caribbean reef shark - 1 According to CFMC 2005. Modified from Garcia-Sais et al. 2010, 2012

García-Sais et al. (2012) characterized the mesophotic habitats at ALS and also conducted an independent fishery survey of commercially important fish and shellfish species. The survey included: queen conch, spiny lobsters, and commercially important fishes such as roupers (red hind, yellowfin, black grouper, and Nassau grouper), snappers (mutton snapper, Cubera snappers, dog snapper, and yellowtail snapper), the queen triggerfish, hogfishes, the lionfish, great barracuda, and nurse sharks. The mean density of queen conch, red hind, hogfish, mutton, dog, and cubera snappers were much higher at ALS than at any other mesophotic system previously studied. The authors suggested that such higher abundance is related to the connectivity of mesophotic habitats at ALS with shallow nearby neritic recruitment habitats than other more oceanic sites such as Desecheo and BS that are separated from the insular shelf by deep oceanic waters.

Ibrahim et al. (2018a) developed an approach for the automatic classification of grouper vocalizations from ambient sounds recorded in situ with fixed hydrophones based on weighted features and a sparse classifier. The dataset used in this research was recorded off the west coast of Puerto Rico at ALS, BS, and Mona Island. Group sounds were labeled initially by humans for training and testing various classification methods. In the feature extraction phase, four types of features were used to identify sounds produced by

groupers. Once the sound features were extracted, three representative classifiers were applied to categorize the species that made these sounds. Experimental results showed that the overall percentage of identification using the best combination of the selected feature extractor weighted Mel frequency cepstral coefficients and sparse classifier achieved 82.7% accuracy. The proposed algorithm has been implemented in an autonomous platform (wave glider) for real-time detection and classification of group vocalizations.

Ibrahim et al. (2018b) investigated the effectiveness of deep learning for the automatic classification of grouper species by their vocalizations. They used wavelet denoising to reduce ambient ocean noise and later used a deep neural network to classify sounds generated by four species of groupers. The dataset used in this research was recorded off the west coast of Puerto Rico at ALS, BS, and Mona Island. Experimental results for the selected species of groupers show that the proposed approach achieves a classification accuracy of around 90% or above in all of the tested cases, a result that is significantly better than the one obtained by a previously reported method for automatic classification of grouper calls (WMFCC, cf. Ibrahim et al. 2018a).

Appeldoorn et al. (2018) analyzed the calling behavior of the red hind to establish temporal patterns by signal type during the lunar spawning cycle. Recordings were obtained from an underwater passive acoustic recorder scheduled to record low-frequency ambient sounds for 20 sec every 5 min. The unit was deployed yearly at ALS. Once they established the type signal, they applied the same analysis to the extended periods of calling activity and used these patterns to infer behavior.

Ibrahim et al. (2019) proposed a method for the classification of call types of the red hind. Two distinct calls of red hind were analyzed. The grouper calls were recorded at ALS and MCD. Experimental results showed that the innovative approach produces superior results in comparison with those obtained by non- ensemble methods. The algorithm reliably classified red hind call types with over 90% accuracy and successfully detected some calls missed by human observers.

Zayas et al. (2020) described vocalizations produced by the red hind and their respective behavioral contexts in the field (using data recorded at ALS) and the laboratory. Five sound types were identified, including four calls recorded in captivity and one sound recorded in the wild, labeled as Chorus. Additionally, the grunt call type recorded was presumed to be produced by a female. Call types consisted of variations and combinations of low frequency (50—450 Hz) pulses, grunts, and tonal sounds in different combinations. Common call types exhibited diel and lunar oscillations during the spawning season, with both field and captive recordings peaking daily at 1800 AST and eight days after the full moon.

3. Tourmaline Bank (TB)

3.1 History and description of TB Tourmaline Bank (Seasonal Fishing Closure Area) was established by the NMFS in 1993 as a part of a rule that intended to protect and conserve the highly exploited reef fish resources of Puerto Rico and the U.S. Virgin Islands (Federal Register 1993). In 1996 NMFS modified the original TB’s limits to their current limits (Federal Register 1996). TB is located both in the EEZ and in the PR’s territorial waters and has a total area of 31.4 km2. The no-take area is 31.3 km2. TB is governed by the Caribbean Fisheries Management Council (CFMC), The National Oceanographic and Atmospheric Agency (NOAA), and the Puerto Rico Department of Natural and Environmental Resources (PR-DNER). TB is a seasonal no-take zone with a closure between December 1 to February 28 (Pittman et al. 2014, Schärer-Umpierre et al., 2014). TB partially coincides with a Puerto Rican marine reserve of Tourmaline.

TB (Seasonal Fishing Closure Area) is located within the 18°11.2′ N 67°22.4′ W; 18°11.2′ N 67°19.2′ W; 18°08.2′ N 67°19.2′ W; 18°06.2′ N to the 67°22.4′ W; 18°11.2′ N 67°22.4′ W (Fig 5). Since 1996, every year, ALS is a no-take area between December 1 and February 28. The Tourmaline Bank (Seasonal Fishing Closure Area) has the following features: site: EEZ (40%) and PR (60%); total area: 31.4 km2; No take area: 31.4 km2; establishment mechanism: MSFC & M Act; governing institutions: NOAA, CFMC, and PR-DNER; level of protection: seasonal no-take zone; timing of closure: December 1 to February 28 (CFMC-NOAA 2009; Pittman et al. 2014, Schärer-Umpierre et al. 2014).

Figure 5. Location of Tourmaline Bank (Seasonal Fishing Closure Area) with the locations of the studies done in the MMA.

3.2 Marine ecosystems present in TB TB is located on the border of the Puerto Rican shelf, offshore Bramadero bay (Cabo Rojo). García-Sais et al. (2013) characterized the main habitats present at TB between 30 and 50 m depth. They recognized five main habitats: sandy substrate, scattered patch reefs surrounded by sand; colonized pavement; algal rhodolith reef deposits; and a slope wall rocky (Fig. 6). Most of these habitats are unconsolidated and abiotic habitats. The sand was the primary substrate type covering 48.1 % of the total study area, yet mostly uncolonized (abiotic)—the sporadic occurrence of interspersed gorgonians and occasional sightings of milk or queen conch. Rhodolith reef deposits were the most prominent benthic habitat present along the western section of the mesophotic outer shelf. They represented the dominant biotic habitat in terms of aerial cover with 37.5 % of the total study area within the 30 – 50 m depth range. Live coral reef habitats within the mesophotic 30 – 50 m depth range were very scarce and only associated with a small yellow-pencil

(Madracis auretenra) biotope growing as a patch the rhodolith reef. Figure 6. Benthic habitat map of the mesophotic region within the 30 – 50 m depth range at Tourmaline Reef, Mayaguez (extracted from García-Sais et al. 2013).

In studies for the PR-DNER, García-Sais et al. (2019) characterized other shallower areas of this reef. Authors found more diverse benthic assemblages composed of stony corals, hydrocorals, sponges, and octocorals. In the section "reported species," a list of the most important species found in TB in the two surveys mentioned is presented.

3.3 Condition and changes through time of marine ecosystems within TB The PR-DNER monitors the shallow and mesophotic reefs of Puerto Rico, and one of its monitoring sites is the shallowest section (10-30 m deep) of TB. The results from this monitoring effort are presented below, both for the benthic community and for the fish associated with the reef.

3.3.1 Benthic community This section of this information compilation is prepared according to the García-Sais et al. 2019´s report. At 10 m depth (Figure 7a), differences of substrate cover by live corals were not statistically significant (ANOVA; p = 0.994). During the 2006 monitoring survey, mean live coral cover declined 22.43%, from 44.14% in 2005 to 34.24%. This decline was measured after the regional coral bleaching event that affected most of the northern Caribbean Sea. The variation in coral cover was not significant due to the high variability (not direction) within transects. At the population level, a decline of live coral cover was found for Orbicella annularis (complex) (ANOVA; p= 0.028), the dominant coral species in terms of reef substrate cover at this depth. Substrate cover by O. annularis declined 46.0% between 2005 and 2006 and was the main driver of the overall decline of live coral at this depth. After 2009, the O. annularis species complex presented a consistent pattern of increasing substrate cover until the 2015 survey. During the 2017 survey, the O. annularis complex exhibited a mild reduction of reef substrate cover, but the variation was statistically insignificant. During the 2019 survey, the mean cover by the Orbicella species complex (10.63%) showed a value similar to that of 2015 (Figure 8a), suggesting that the small decline measured in the previous 2017 survey was probably an artifact of sampling variability.

At 20 m, cover by hard corals showed a gradual decline from a baseline mean of 31.79 % in 2004 to 22.80% in 2007 (Figure 7b). Such reduction was probably associated with coral bleaching-induced mortalities after the regional event of late August 2005, with prolonged effects down to 2008. After 2010 live coral cover maintained an increasing trend until the previous 2017 survey, evidencing a recovery of 34.45 % from its lowest cover in 2010 and approaching its baseline cover at 31.79%. Differences associated with this recuperation trend were statistically significant (ANOVA, p = 0.028). During the 2019 survey, mean substrate cover by hard corals registered a 10.4% decline from the previous study of 2017, but such differences were statistically insignificant. The combined substrate cover by Orbicella spp, previously described as the O. annularis complex, was the main driver of the declining trend of live coral between 2004 and 2007 and its recent recovery because it is the dominant coral species complex at this depth (Figure 8b). During the 2019 survey, the combined cover by Orbicella spp. (22.04%) declined 7.89% from the mean cover in 2017 (23.78%). From the reef stations monitored so far, this depth exhibited the highest coral disease prevalence (9.5%), and several colonies of O. faveolata were observed to be suffering from infectious diseases.

At 30 m, differences of hard coral cover between monitoring surveys were statistically significant (ANOVA; p = 0.016). Coral cover remained stable during 2004 and 2010. Since then, an increase in live coral cover was found until the previous 2017 survey. Coral cover increased from 13.54% during the baseline survey to 23.71% in 2017 (Figure 7c). The coral cover increase was due to two dominant corals, the Agaricia spp assemblage, of which A. grahamae was the main component, and Orbicella faveolata (Figure 8c). Since the baseline survey in 2004, many large colonies of Orbicella spp. were already dead and overgrown by turf algae, indicative of major stress acting over this coral species (complex) sometime

before our baseline survey. Hard coral has re-colonized (previously) dead coral sections by displacing turf algae, which have shown a corresponding declining trend of reef substrate cover over time. The mean cover of 21.48% measured during the present 2019 survey represents a decline of 9.40% from the previous 2017 survey. This difference was statistically insignificant.

Figure 7. Monitoring trends (1999 – 2019) of mean substrate cover by sessile-benthic categories at Tourmaline Bank. a 10 m, b 20 m, c 30 m (from García-Sais et al. 2019).

* Note that previous to 2019, all three Orbicella species were documented under ”Orbicella annularis complex”. In 2019, Orbicella complex were divided by species, which can be seen in this graph. 1 Orbicella annularis, 2 O. annularis complex, 3 O. faveolata, 4 O. franksi, 5 Montastraea cavernosa, 6 Porites porites, 7 P. astreoides, 8 Agaricia agaricetes, 9 Agaricia spp, 10 Colpophyllia natans, 11 Siderastrea siderea, 12 Pseudodiploria strigosa, 13 Stephanocoenia intersepta, 14 Madracis formosa, 15 M. aurentenra, 16 Dendrogyra cylindrus.

Figure 8. Monitoring trends (1999 – 2019) of mean substrate cover by hard coral species at Tourmaline Bank. a 10 m, b 20 m, c 30 m (from García-Sais et al. 2019).

3.3.2 Reef fish At 10 m, minimum mean values of fish density and species richness were observed during 2008, when mean density declined 31.4 % relative to the baseline survey (Figure 9a). Density differences between annual surveys were statistically significant (ANOVA; p< 0.0001). Schooling zooplanktivores influenced fish density at this depth with highly aggregated distributions, such as the blue chromis (Chromis cyanea), masked goby (Coryphopterus personatus), and creole wrasse (Clepticus parrae). Inter-annual fluctuations of these species appear to be related to density-independent factors and physical conditions at the survey time. C. personatus is a schooling species with highly aggregated distributions and dominant within belt- transects. Such aggregated distributions introduce high sampling variability. Many observations are needed within a reef system to detect temporal density patterns. Differences in fish species richness between surveys were statistically significant (ANOVA; p < 0.0001), driven by a severe decline of species during 2008 and 2017 relative to all other surveys. Such declines coincided with low densities of C. personatus and/or C. parrae. Density fluctuations of these forage species may be related to ecological (interaction type predator-prey) or abiotic factors (physical conditions associated with wave action impact an assemblage of small fishes that cannot withstand the surge effect related to intense wave action and are displaced from the

shallow reef). During the 2019 survey, both mean fish density and species richness increased relative to the previous 2017 survey but still fell within the lower range of the historical means for both parameters.

Figure 9. Monitoring trends (1999 – 2019) of mean fish density and species richness within 3x10 m belt-transects at Tourmaline. a 10 m, b 20 m, c 30 m (from García-Sais et al. 2019).

At 20 m, differences in fish density and species richness between monitoring surveys were statistically significant (ANOVA; p < 0.0001). Density variations were associated with density peaks in 2005, 2006, 2008, 2011, and 2015 relative to other monitoring surveys (Figure 9b). Such density peaks were driven by high densities of masked goby (Coryphopterus personatus). A sharp, consistent decline of species richness

was observed after the coral bleaching event of late 2005 with lingering effects until 2008. The bleaching event severely affected the amount of live coral and perhaps corresponding implications to fish recruitment and residential habitats. The mean fish density measured during the 2019 survey (67.2 Ind/30m2) fell within the low range of densities previously measured at this depth, influenced by a low density of C. personatus relative to other surveys. Mean species richness in 2019, however, increased 8.5% from the previous 2017 survey. The mean fish density and species richness were within one standard deviation of the mean during 2019.

At 30 m, differences in fish density and species richness between annual surveys were statistically significant (ANOVA; p < 0.0001). Density differences between monitoring surveys were driven mainly by the fluctuations of masked goby (Coryphopterus personatus). Consistent with the previous 2017 survey, the density of masked goby was low again in 2019, influencing the difference of total fish density relative to previous surveys. Annual fluctuations of species richness did not show any consistent pattern through time and may be related to variable physical conditions at the time of surveys (Figure 9c).

3.4 Reported species within TB At TB, two types of surveys have been carried out, one focused on the communities present between 30 and 50 m (study for the CFMC) and the second focused on the communities present at 10, 20, and 30 m depth (data from the PR-DNER). Below we summarized the results of both studies. One hundred and two benthic species have been reported from TB, composed of cyanobacteria and algae, sponge, scleractinian corals, hydrocorals, and octocorals (Table 5). The most abundant benthic species/taxonomic group are algal turfs and the macroalgae Lobophora variegata; the most speciose group is the sponges. Among the scleractinian corals, the most representative species are Agaricia sp., Montastraea cavernosa, Tubastraea coccinea and Orbicella spp.

The fish community at TB is composed of 110 species (Tables 6 and 7). Table 6 shows the commercially important fish species found at this site with their fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005), conservation status according to the IUCN red list, and trophic group according to Ennis et al. (2019). In the case of CFMC’s FMU, only those categories that include the largest or most important fish from the commercial point of view have been included in this table. The commercially important species registered at ALS are groupers (red hind, coney, graysby) and snappers (blackfin snapper, mutton snapper, and dog snapper). Table 7 shows other representative fish species found at this site and their fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005). In 2012, the lionfish was well established at this marine reserve, as it is inferred by its frequency distribution across the different reef habitats, length frequency distribution, and density (García-Sais et al. 2013).

Table 5. Most representative benthic species at the TB. Species/Groups Type Species/Groups Type Acropora cervicornis Scleractinian Porites duvaricata Scleractinian Agaricia agaricites Scleractinian Porites porites Scleractinian Agaricia fragilis Scleractinian Pseudodiploria strigosa Scleractinian Agaricia grahamae Scleractinian Siderastrea siderea Scleractinian Agaricia lamarckii Scleractinian Stephanocoenia intercepta Scleractinian Colpophyllia natans Scleractinian Millepora alcicornis Hydrocoral

Dendrogyra cylindrus Scleractinian Briareum asbestinum Octocoral Diploria labyrinthiformis Scleractinian Erythropodium caribaeorum Octocoral Eusmilia fastigiata Scleractinian Eunicea spp. Octocoral Helioseris cucullata Scleractinian Muricea sp. Octocoral Madracis auretenra Scleractinian Pseudoplexaura spp. Octocoral Madracis carmabi Scleractinian Agelas conífera Sponge Madracis decactis Scleractinian Neopetrosia spp. Sponge Meandrina meandrites Scleractinian Plakortis spp. Sponge Montastraea cavernosa Scleractinian Dictyota spp. Macroalgae Orbicella annularis Scleractinian Halimeda spp. Macroalgae Orbicella faveolata Scleractinian Lobophora variegata Macroalgae Orbicella franksi Scleractinian Peyssonnelia spp. Macroalgae Porites astreoides Scleractinian Ramicrusta spp Macroalgae Porites dIvaricata Scleractinian Turf algae Turf Porites porites Scleractinian Cyanobacteria Cyanobacteria *Data from García-Sais et al. 2007, 2019.

Table 6. Representative commercially important fish species at TB. Scientific Name Common Name Fisheries2 UICN Red List Status3 Trophic Group1 Epinephelus guttatus Red hind Groupers Least Concern Invertivore Cephalopholis fulva Coney Groupers Least Concern Piscivore Cephalopholis cruentata Graysby Groupers Least Concern Piscivore Lutjanus buccanella blackfin snapper Snappers Least Concern Piscivore Lutjanus analis Mutton snapper Snappers Least Concern Piscivore Lutjanus jocu Dog snapper Snappers Data Deficient Piscivore Ocyurus chrysurus Yellowtail snapper Snappers Data Deficient Planktivore Caranx crysos Blue runner Jacks Least Concern Piscivore Caranx lugubris Black jack Jacks Least Concern Piscivore Caranx ruber Bar jack Jacks Least Concern Piscivore Seriola dumerili Greater amberJack Jacks Least Concern Piscivore Seriola rivoliana Almaco Jack Jacks Least Concern Piscivore Balistes vetula Queen trigger Triggerfish Near Threatened Invertivore Pomacanthus arcuatus Gray angel Angelfish Least Concern Spongivore Pomacanthus paru French angelfish Angelfish Least Concern Spongivore Holacanthus ciliaris Queen angel Angelfish Least Concern Spongivore Sparus guacamaia Rainbow parrotfish Parrotfishes Near Threatened Herbivore Scarus iseri Striped parrotfish Parrotfishes Least Concern Herbivore

1 García-Sais et al. 2007 and 2019; 2 According to CFMC 2005; 3 According to UICN Red List Status

Table 7. Other fish species at TB. Scientific Name Common Name Fisheries1 Lutjanus cyanopterus Cubera Snapper Snapper Scomberomorus cavalla King mackerel - Pseudupeneus maculatus Spotted goatfish Goatfish Holocentrus adcensionis Longjaw Squirrelfish Squirrelfish Holocentrus rufus Longspine Squirrelfish Squirrelfish Malacanthus plumieri Sand Tilefish Tilefish Halichoeres cyanocephalus Yellowcheeck Wrasse Wrasse Lachnolaimus maximus Hogfish Wrasse Holocentrus rufus Longspine squirrelfish Squirrellfish Acanthurus bahianus Ocean surgeon Surgeonfish Acanthurus chirurgus Doctorfish Surgeonfish Dasyatis americana Southern Stingray - Elagatis bipinnulata Rainbow runner Jack Bodianus rufus Spanish hogfish Wrasses Sphyraena barracuda Great barracuda - Pterois volitans Lionfish - Ginglymostoma cirratum Nurse shark - Negaprion brevirostris Lemon shark - 1 According to CFMC 2005. Data from García-Sais et al. 2007, 2019.

3.5 Primary scientific studies that have or are taking place within TB TB is part of the Puerto Rico Coral Reef Monitoring Program (PR-CRMP) sponsored by NOAA/CRCP and administered by the PR-PRDNER. This program started in 1999 with baseline characterizations of reef substrate cover by sessile-benthic categories and determinations of fish and motile megabenthic invertebrate taxonomic composition and densities (García-Sais et al. 2019). By 2015, surveys were conducted on a total of 15 reefs within TB. That monitoring program produced the information presented in section 3.3 of this report.

García-Sais et al. (2013) characterized the mesophotic sector of TB. Also, they conducted an independent fishery survey of commercially important fish and shellfish species. This survey included: queen conch, Spiny lobsters, and some commercially important fishes. Mutton, blackfin, dog and cubera snappers, red hinds, lionfish, hogfish, and queen triggerfishes were the most abundant of the large demersal commercially important fishes present within the mesophotic habitats of Tourmaline Bank. The mean density of queen conch, hogfish, mutton, dog, and cubera snappers was much higher at Tourmaline and Abrir La Sierra than at mesophotic systems previously studied. The authors suggested that such higher abundance is related to high connectivity to nearby shallow recruitment habitats than oceanic sites (i.e., Desecheo and Bajo de Sico) separated from the insular shelf by deep ocean waters.

4. Bajo de Sico (BS) 4.1 History and description of BS The NMFS established in 1996 the seasonal closure in the vicinity of "Bajo de Sico." The intended effect of this rule was to protect red hind (Epinephelus guttatus) spawning aggregations by prohibiting fishing in these areas during the spawning season (Federal Register 1996). The seasonal closure was initially proposed between December 1 and February 28 of each year. BS (Seasonal Fishing Closure Area) is located at 18°15.7′ N 67°26.4′ W; 18°15.7′ N 67°23.2′ W; 18°12.7′ N 67°23.2′ W; 18°12.7′ N 67°26.4′ W; 18°15.7′ N 67°26.4′ W (Fig 10). In 2010 NMFS modified the Bajo de Sico seasonal closure from a 3-month closure to a 6-month closure and prohibited fishing for and possession of Caribbean reef fish in or from the exclusive economic zone (Federal Register 2010). This final rule also banned anchoring in the EEZ portion of Bajo de Sico year-round. The intended effect of this rule was to provide further protection for red hind spawning aggregations and large snappers and groupers and better protect the essential fish habitat (EFH) where these species reside (Federal Register 2010). Since 2010, every year, BS is a seasonal no-take area between October 1 and March 31.

Bajo de Sico (Seasonal Fishing Closure Area) has the following features: site: EEZ (60%) and PR (40%); total area: 31.4 km2; No take area: 31.4 km2; establishment mechanism: MSFC & M Act; governing institutions: NOAA, CFMC, and PR-DNER; level of protection: seasonal no-take zone; timing of closure: October 1 to March 31 (CFMC-NOAA 2009; Pittman et al. 2014, Schärer-Umpierre et al. 2014).

Figure 10. Location of Bajo de Sico (Seasonal Fishing Closure Area).

4.2 Marine ecosystems present in BS

Bajo de Sico (BS) is a seamount located in Mona Passage, about 27 kilometers off Mayagüez in the west coast of Puerto Rico (García-Sais et al. 2007) (Fig 10). BS is part of a ridge, known as the great southern Puerto Rico fault zone (Garrison and Buell 1971 in García-Sais et al. 2007), a submerged section of the Antillean ridge extending across the entire Mona Passage, connecting Puerto Rico with La Hispaniola. BS has a maximum length of approximately 6.0 km along its southwest to the northeast axis and a width of about 2.5 km across the northwest to the southeast axis. The total surface area of the seamount within the 100 m depth contour is approximately 11.1 km2 (García-Sais et al. 2007) (Figure 11).

García-Sais et al. (2007) characterized the main habitats present at BS between 30 and 50 m depth. They found: a reef top and a vertical reef wall associated with rock promontories, colonized pavement and sand channels at the base of promontories, uncolonized gravel and rhodoliths at the reef slope, and a colonized rhodolith reef habitat surrounding the rock promontories at least to a depth of 50 m (Figure 11). Benthic habitats beyond 50 m were not field verified. Several video images generated by the R/V Nancy Foster showed coral growth down to a maximum depth of 90 m and the deep shelf platform at BS (García-Sais et al. 2007).

The sessile-benthic community at the reef top was characterized by a highly diverse assemblage comprised of benthic algae (52%), sponges (26%), scleractinian corals (8%), octocorals (5%), and hydrozoans (3%), with an abiotic cover of less than 1.5% (García-Sais et al. 2007).

Figure 11. Benthic habitat map of Bajo de Sico up to a maximum depth of 50 m (García-Sais et al. 2007).

The reef wall habitat was characterized by irregular formations with deep crevices, undercuts, gaps, ledges, and other substrate irregularities. The sessile-benthos of the reef wall habitat was also highly and taxonomically diverse, comprised of sponges (43%), benthic algae (26%), octocorals (14%), scleractinian corals (5.5%), antipatharians (3%), and hydrozoans (2%). The abiotic cover was approximately 4%. (García-Sais et al., 2007). The deep platform rhodolith reef, at least down to the maximum surveyed depth of 50 m, appears to be a vast deposit of crustose algal nodules or rhodoliths overgrown by a dense macroalgal carpet, mostly the encrusting fan-leaf alga, Lobophora variegata. The sessile-benthic invertebrate community was characterized by relatively low taxonomic diversity (García-Sais et al., 2007).

4.3 Condition and changes through time of marine ecosystems within BS García-Sais et al. (2007) characterized the benthic ecosystems present at BS. No other study has been conducted since then. Thus the current state or any change through time is unknown in this Marine Managed Area.

4.5 Reported species within BS The characterization carried out by García-Sais et al. (2007) of the mesophotic habitats present at BS recorded 109 species/taxonomic groups of benthic algae, sponge, scleractinian corals, hydrocorals, and octocorals. The most abundant benthic species/taxonomic groups were algal turfs and the macroalgae Lobophora variegata; among the scleractinian corals, the most representative species were Agaricia agaricetes, Porites astreoides, and Tubastrea coccinea. Table 8 shows the most representative benthic species and groups.

García-Sais et al. (2007, 2012) recorded 79 fish species at BS. Table 9 contains information of interest on the most representative commercially important fish species found at this site; i.e., name (scientific and common), fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005), conservation status according to the IUCN red list and trophic group according to Ennis et al. 2019. In the case of CFMC´s FMU, only those categories that include the largest or most important fish from the commercial point of view have been included in this table. The most commercially important species registered at ALS were: some groupers (red hind, Nassau, yellowfin grouper, coney, graysby) and snappers (schoolmaster, mutton snapper).

Table 10 shows information of other representative fish species found at this site, i.e., name (scientific and common) and fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005). It should be noted that in 2012 the presence of the lionfish was already registered in this marine reserve.

Table 8. Most representative benthic species recorded at Bajo de Sico. Species/Groups Type Species/Groups Type Agaricia agaricites 1 Scleractinian Porites astreoides Scleractinian Agaricia grahamae 1 Scleractinian Pseudodiploria strigosa @ Scleractinian Agaricia lamarcki 1 Scleractinian Scolymia cubensis Scleractinian Colpophyllia natans Scleractinian Siderastrea siderea Scleractinian Dichocoenia stokesi Scleractinian Stephanocoenia michelini Scleractinian Diploria labyrinthiformis Scleractinian Tubastrea coccinea Scleractinian Eusmilia fastigiata Scleractinian Millepora alcicornis Hydrocoral Helioseris cucullata @ Scleractinian Stylster roseus Hydrocoral Isophyllia sinuosa Scleractinian Iciligorgia schrammi Octocoral Isophyllastrea rigida Scleractinian Pseudopterigorgia sp. Octocoral Leptoseris cailleti Scleractinian Agelas clathrodes Sponge Madracis decactis Scleractinian Agelas conifera Sponge Meandrina meandrites Scleractinian Aplysina cauliformis Sponge Montastraea cavernosa Scleractinian Xestospongia muta Sponge Mycetophyllia aliciae Scleractinian Lobophora variegata Macroalgae Mycetophyllia lamarckiana Scleractinian Halimeda spp. Macroalgae Oculina varicosa Scleractinian Turf algae Turf Orbicella annularis @ Scleractinian Filamentous cyanobacteria Cyanobacteria

@ Shows the valid and updated name of the species. Data from García-Sais et al. 2007.

Table 9. Commercially important fish species recorded at Bajo de Sico. UICN Red List Trophic Scientific Name Common Name Fisheries2 Status3 Group1 Epinephelus guttatus Red hind Groupers Least Concern Invertivore Epinephelus striatus Nassau grouper Groupers Critically Endangered Invertivore Mycteroperca venenosa Yellowfin grouper Groupers Near Threatened Piscivore Mycteroperca tigris Tiger grouper Groupers Data Deficient Piscivore Cephalopholis fulva Coney Groupers Least Concern Piscivore Cephalopholis cruentata Graysby Groupers Least Concern Piscivore Lutjanus cyanopterus Cubera snapper Snappers Vulnerable Piscivore Lutjanus analis Mutton snapper Snappers Least Concern Piscivore Lutjanus apodus Schoolmaster Snappers Least Concern Piscivore Lutjanus jocu Dog snapper Snappers Data Deficient Piscivore Ocyurus chrysurus Yellowtail snapper Snappers Data Deficient Planktivore

Caranx crysos Blue runner Jacks Least Concern Piscivore Caranx lugubris Black jack Jacks Least Concern Piscivore Caranx ruber Bar jack Jacks Least Concern Piscivore Calamus pennatula Pluma porgy Porgies Least Concern Invertivore Balistes vetula Queen trigger Triggerfish Near Threatened Invertivore Pomacanthus paru French angelfish Angelfish Least Concern Spongivore Holacanthus ciliaris Queen angel Angelfish Least Concern Spongivore Sparisoma aurofrenatum Redband parrotfish Parrotfishes Least Concern Herbivore Sparisoma viride Stoplight parrotfish Parrotfishes Least Concern Herbivore 1 From Ennis et al. 2019; 2 According to CFMC 2005; 3 According to UICN Red List Status. Modified from Garcia-Sais et al. 2007, 2012.

Table 10. Other representative fish species recorded at Bajo de Sico. Scientific Name Common Name Fisheries1 Calamus calamus Saucereye porgy Porgies Scomberomorus regalis Cero - Pseudupeneus maculatus Spotted goatfish Goatfish Mulloidichthys martinicus Yellow goatfish Goatfish Anisotremus surinamensis Black margate Grunts Anisotremus virginicus Porkfish Grunts Haemulon sciurus Bluestriped grunt Grunts Lachnolaimus maximus hogfish Wrasse Holocentrus rufus Longspine squirrelfish Squirrellfish Acanthurus bahianus Ocean surgeon Surgeonfish Acanthurus chirurgus Doctorfish Surgeonfish Acanthurus coeruleus Blue tang Surgeonfish Melichthys niger Black durgon Triggerfish Bodianus rufus Spanish hogfish Wrasses Sphyraena barracuda Great barracuda - Pterois volitans Lionfish - Ginglymostoma cirratum Nurse shark - Negaprion brevirostris Lemon shark - 1 According to CFMC 2005. Modified from Garcia-Sais et al. 2007, and 2012.

4.6 Primary scientific studies that have or are taking place within BS The scientific studies that have been conducted within BS are related to developing new methodologies to understand spawning aggregations of several grouper species within BS. The most recent studies carried out at BS, and their main findings are summarized below.

Schärer-Umpierre et al. (2012b) described sound production by Nassau grouper (Epinephelus striatus) from four different spawning aggregation sites in the Caribbean (BS, GB, and Red Hind Marine Conservation District were included in this study). Passive acoustic data and video were recorded in Belize (February 2011) and Puerto Rico (February 2012), revealing two distinctive sounds. The first is a pulse train sound associated with an alarm or warning behavior, while the second is a tonal sound associated with reproductive behaviors, including courtship displays. The average peak frequency of the pulse train was 77.4 ± 30.3 Hz, individual pulse duration was 0.09 ± 0.02 s, and the number of pulses varied from 6 to 13.

The average peak frequency was 99.0 ± 33.6 Hz for the tonal sound, and the sound duration was 1.6 ± 0.3 s, ranging from 0.9 to 2.3 s. Long-term recordings at the Grammanik Bank, US Virgin Islands (February 2011) revealed variability in the daily patterns of tonal sounds during the residence time at the aggregation. Sound production was highest 7 to 8 days after the full moon between 20:00 and 21:00 h Atlantic Standard Time. The Nassau grouper courtship-associated sounds provide a valuable tool to study the dynamics of spawning aggregations critical for the recovery of this Endangered species.

Schärer-Umpierre et al. (2014) carried out passive acoustic and synchronous video recordings at two spawning aggregation sites (BS and Mona Island) to study the sounds associated with reproductive behaviors of black grouper (Mycteroperca bonaci). A characteristic sound was produced during courtship displays involving behaviors commonly observed for groupers of this genus at aggregations. The sound has a short pulsing section followed by a more extended tonal portion with a mean peak frequency below 100 Hz. Courtship-associated sounds were quantified over one spawning season at Mona Island, Puerto Rico. Most of the daily sound production occurred during a period of 2 h before sunset. The highest rates of the sound output lasted for ten days with lunar periodicity over three consecutive months coincident with the reported season of reproduction. Passive acoustics provide a tool to measure the variability of the reproductive activity of M. bonaci over time. They may provide a method to evaluate current strategies designed to protect multi-species spawning aggregations critical for the recovery of threatened groupers.

Jackson et al. 2014 studied the Nassau grouper (Epinephelus striatus) genetic connectivity across the Caribbean, analyzing genetic variation in mitochondrial DNA (mtDNA), microsatellites, and single nucleotide polymorphisms (SNPs). Sampling sites at GB and Bajo de Sico were part of this study. It was found evidence of genetic differentiation across the Caribbean Sea of this grouper using mtDNA (FST =

0.206, p<0.001), microsatellites (FST = 0.002, p = 0.004) and SNPs (FST = 0.002, p = 0.014), and identified three potential barriers to larval dispersal. Genetically isolated regions identified mirror those seen for other invertebrate and fish species in the Caribbean basin. The study detected the strongest barrier in the Bahamas, isolating the western sites from those in the central and eastern Caribbean. However, it was unable to detect a genetic break between populations on either side of the Mona Channel (western Puerto Rico). Oceanographic regimes in the Caribbean may largely explain patterns of genetic differentiation among Nassau grouper subpopulations. Study results nonetheless found key insights into the vulnerable status of Nassau grouper throughout its geographic range. If subpopulations represented by spawning aggregations are heavily reliant upon self-recruitment and adults are faithful to specific aggregations, as tagging data suggest, then their persistence, and that of the subpopulations that form them may rely upon fisheries management and conservation efforts focusing on the maintenance of local genetic diversity and implementing management units at the appropriate spatial scale suggested by genetic data. Regional patterns of genetic differentiation observed may also warrant standardization of fisheries management and conservation initiatives, particularly among countries within genetically isolated regions.

Tuohy et al. (2015) carried out the first known application of in situ tagging performed at mesophotic depths. The authors used closed-circuit rebreather (CCR) technology to tag ten Nassau groupers at 40 – 50 m depth at BS, a recognized spawning aggregation site off the west coast of Puerto Rico. The total time (time divers arrived at the trap to time of release) for each procedure was approximately 12 min. All fish were released and observed without indication of stress or physiological impairment. Short-term tracking of tagged fish revealed a 100% post-surgery survival rate with maximum detection of 347 days post- surgery. Survival rates of this nature have not been quantified or reported from other tagging studies, allowing the researchers to conclude that this methodology, coupled with the efficiency provided by CCR at these depths, enhanced survivorship and bias for studies utilizing acoustic telemetry.

Rowell et al. (2018) identified a new sound produced by Nassau Grouper (Epinephelus striatus) in association with, although potentially not exclusive to, an agonistic interaction at a spawning aggregation. Asynchronous audio—video recorder was deployed at BS at a depth of 50 m. The authors also provided a behavioral and acoustic description for the identification of this sound in future studies. The discovery of a third sound produced by Nassau Grouper further highlights the importance of acoustic communication coupled with visual displays in fishes and enhances our ability to decipher patterns of different behaviors. Furthermore, identifying a new sound increases the ability to document the presence of this endangered species at spawning sites. Future efforts may reveal that the sound is produced within additional behavioral contexts during and outside the spawning season, such as the defense of territories or food resources. Continued efforts to catalog the sounds and behaviors of species like Nassau Grouper will increase our ability to monitor and understand fish behaviors.

Ibrahim et al. (2018a) presented an approach for the automatic classification of grouper vocalizations from ambient sounds recorded in situ with fixed hydrophones based on weighted features and sparse classifier.

The dataset used in this research was recorded off the west coast of Puerto Rico at ALS, BS, and Mona Island. See findings presented in section 3.6.

Schärer-Umpierre et al. (2019) recorded a low amplitude and potentially courtship-related sound produced by invasive lionfish (Pterois spp.), the first reported sound by lionfish in the wild. The behavior and associated sounds were recorded in the presence of multiple lionfish in both Puerto Rico (BS) and the Florida Keys during separate research projects. The authors provided a brief characterization of this behavior and sound. Lionfish are known to produce sounds, but the behavior associated with sound production in natural conditions has not been previously documented.

5. Grammanik Bank (GB)

5.1 History and description of GB Grammanik Bank (Seasonal Fishing Closure Area) was established by NMFS via the MSFC & M Act in 2005 to improve fisheries management, emphasizing protecting spawning aggregations of yellowfin grouper (Mycteroperca venenosa). GB is located in the EEZ with a total area of 1.5 km2. The no-take area is 1.5 km2. GB is governed by the Caribbean Fisheries Management Council (CFMC), The National Oceanographic and Atmospheric Agency (NOAA), and the Virgin Islands Department of Natural Resources (VI-DPNR). GB is a seasonal no-take zone with a closure between February 1 to April 30 (Pittman et al. 2014, Schärer-Umpierre et al. 2014).

GB is located south of St. Thomas on the border of the Puerto Rican shelf, next to Anegada Passage (Figure 11). The bank is made up of a main (primary) bank, to the south, and a second bank, to the north, separated each other by a narrow sand channel (approximately 20-30 m wide) (Herzlieb et al. 2006, Smith et al. 2008). The top of the bank runs in a roughly east-west direction in 35-40 m of water and extends 1.69 km at its longest point (between 18º11.30N, 064º57.50W, and 18º11.60N, 064º56.60W), and 100 m wide for virtually its whole length (Nemeth et al. 2006).

Grammanik Bank (GB) is the most studied Marine Managed Area in the US Caribbean. GB is a deepwater reef at the southern edge of the insular Puerto Rican shelf approximately 12 km south of St. Thomas, U.S.VI (Kadison et al. 2006) (Figures 11 and 12). Associated to this bank there is a no-take Marine Managed Area designated based on the Magnuson Stevens Fishery Conservation and Management Act and reauthorizations, which are managed by the CFMC. Currently, GB is recognized as a multispecies Fish Aggregation Area (FSA) for M. venenosa and several other grouper species (Epinephelus striatus, M. tigris, M. interstitialis), snappers (Lutjanus jocu and L. cyanopterus), and Bermuda chub (Kyphosus saltatrix) (Nemeth et al. 2006a, Kadison et al. 2010, Kadison et al. 2011, Nemeth and Kadison 2013, Biggs and Nemeth 2016).

GB was discovered as a grouper, snapper, and parrotfish aggregation area by fishermen in the mid-1950s (Nemeth et al., 2006), and it was fished very lightly until 1990 when an area of 8 km west of the GB – known as the Marine Conservation District (MCD)– was closed seasonally and then year-round to fishing by the Caribbean Fisheries Management Council (CFMC). With the closure of the MCD pressure shifted to the GB (Kadison et al. 2006). The fishing pressure increased grouper landings from GB in excess of 20,000 lbs annually from 1999-200, mostly during spawning aggregations (from February through April) (cf. Kadison et al. 2006).

According to the 2004 Federal Register, underwater visual censuses carried out by researchers at the University of the Virgin Islands (UVI) in March 2002 and 2003, revealed small numbers (i.e., 50 to 60) of the yellowfin grouper (Mycteroperca venenosa) during the peak spawning period. Given the sharp reduction, UVI researchers expressed concern about the high mortality of this grouper and recommended a management action during the peak spawning period. In 2004, the CFMC recommended National Marine Fisheries Service (NMFS) to implement measures to protect a yellowfin grouper (M. venenosa) spawning aggregation and reduce overfishing at GB.

In 2004, the NMFS issued a rule prohibiting fishing or possessing any fish species, except highly migratory species, within the GB (Seasonal Fishing Closure Area) from February 1, 2005, through April 30, 2005 (Federal Register 2005). The GB (Seasonal Fishing Closure Area) is bounded by the following coordinates (Fig 11): A 18°11.898' N 64°56.328' W; B 18°11.645' N 64°56.225' W; C 18°11.058' N 64°57.810' W; D 18°11.311' N 64°57.913' W). Since then, every year the GB is a no-take area between February 1 and April 30. In this context, the term “fish” means finfish, mollusks, crustaceans, and all other forms of marine animal and plant life other than marine mammals and birds. In addition, the term ‘‘highly migratory species’’ means bluefin, bigeye, yellowfin, albacore, and skipjack tunas; swordfish; sharks (listed in appendix A to 50 CFR part 635); white marlin, blue marlin, sailfish, and long bill spearfish (Federal Register, 2005).

Figure 11. Location of the Grammanik Bank (Seasonal Fishing Closure Area).

5.2 Marine ecosystems present in GB GB has historically been defined as a Mesophotic Coral Ecosystem (MCE) (Smith et al. 2011). The bank includes mesophotic coral reef banks, hard bottom sparsely colonized with isolated coral colonies and sponges, and sand channels (Herzlieb et al. 2006, Smith et al. 2008). GB is dominated by Orbicella spp (formerly Montastraea spp.); however, there is representation by a high number of other scleractinian corals that are also present in shallow water reefs (Ennis et al. 2019). In the steep slopes and walls fringed Agaricia

spp are the dominant species. The hard bottoms harboring mixed communities of sponge and macroalgae (mainly Lobophora variegata, epilithic and crustose algae) (Ennis et al. 2019).

Figure 12. Location of Grammanik Bank and Red Hind Marine Conservation District (Smith et al. 2010). The positions of the three permanent TCRMP sites located in this area are indicated as follows: Grammanik Bank Tiger (purple diamond), College Shoal East (blue circle), and Hind Bank East (red star).

5.3 Condition and changes through time of marine ecosystems in GB The U.S. Virgin Islands Territorial Coral Reef Monitoring Program (TCRMP) is in charge of the coral reef management and research in the U.S. Virgin Islands. The TCRMP was implemented by the government of the U.S. Virgin Islands (U.S.V.I), in coordination with the NOAA Coral Reef Conservation Program and the University of the Virgin Islands (UVI). The TCRMP has established baseline states and temporal trends of coral reefs and fish populations and has identified threats to the future of USVI coral reefs. The TCRMP also provides information on land-based sources of pollution, coral bleaching, and fisheries status since its inception in 2001. The program performs annual to semi-annual assessments of benthic community structure, coral health, fish community structure, and physical dynamics at an increasing number of long- term monitoring sites, down to 65 m (220 ft) depth throughout the U.S.VI. The TCRMP, monitored by UVI scientists, has a permanent sampling site named “Grammanik Tiger site”, 38 m depth, at 18,18885 N and - 64,95659 W (Ennis et al. 2019), and has been monitored since 2003, with permanent transects installed in 2007. By 2019 the program has 33 long-term monitoring sites.

According to the 2019 TCRMP report (Ennis et al. 2019), the condition of marine ecosystems at Gammanik Tiger site has changed over time. The cover of Orbicella spp (the most abundant coral) has decreased (~15%), which may reflect the impact of generally higher prevalence of coral diseases at this site (which traditionally had had high coral cover) and a mild bleaching event that occurred in 2012. The benthic area left by dead corals is now colonized by macroalgae.

Figure 13 shows bleaching prevalence (proportion of colonies affected) and bleaching extent (the degree to which a colony is affected) at TCRMP sites (Ennis et al., 2019). In the case of the Grammanik Tiger site, the 2005 event was the strongest with a prevalence of 10% and an extent of almost 70%. In turn, the events of 2010 and 2019, although with higher prevalence, had a much lower extent. The 2019 bleaching event had a prevalence of 40% and an extent of less than 15%.

According to Ennis et al. (2019), the main threats at Grammanik Tiger site are i) Chronic coral white diseases. ii) Periodic disease outbreaks followed by coral bleaching. iii) The dense populations of the invasive lionfish (Pterois volitans) affecting native fish populations.

Figure 13. Coral bleaching prevalence and extent for TCRMP in 2005, 2010, and 2019. Bleaching prevalence is the proportion of the community showing some level of bleaching. Bleaching extent is the mean proportion of the colony area affected by bleaching. Not all sites were sampled prior to 2019. Not all sites were sampled at the peak of the heat stress and may have underestimated bleaching responses for a given year. Reanalyzed data from Ennis et al. 2019.

5.3.1 Benthic community structure Boulder star corals (Orbicella spp.) dominate the coral community of the Grammanik Tiger site; however, there is representation by a high number of other coral species that are also present in shallow-water reefs. Grammanik Tiger lost a moderate amount of its coral cover in the 2005 bleaching event but had not regained any cover by 2011 (figure 14a). Other prominent members of the sessile epibenthic animal community are sponges. The macroalgae Lobophora variegata and epilithic algae dominate the algal community. Both algal groups experienced wide cover variations during monitoring. Macroalgae exhibited their largest cover increases after the bleaching events of 2005, 2012, and 2019 (figure 14b) (Ennis et al., 2019).

5.3.2 Coral Health Ennis et al. (2019), summarize the main changes in coral health at Grammanik Tiger site during monitoring as follows Grammanik Tiger site: Coral health was very affected by bleaching in 2005, but was underestimated in the surveys conducted. The 2010 and 2019 bleaching events did not reveal bleaching detectable above background levels. The high prevalence of bleaching in normal years was due largely to granular bleaching of Orbicella spp., where pigmented spots are surrounded by bleached areas. Figure 14c shows bleaching prevalence and bleaching extent. Coral diseases were prevalent with a high incidence of white disease. Yellow band disease was also reported at high prevalence in the first years of monitoring. Stony coral tissue loss disease (SCTLD) appeared at the site by February 2020 but had not yet had a significant impact on the coral cover. Figure 14d shows disease prevalence. Partial mortality was low but increased rapidly after the 2005 coral bleaching event. Recent partial mortality is high and mainly caused by disease lesions, predations, and fish bites. Figure 14e shows old and recent mortality prevalence.

5.3.3 Reef fish The main documented changes in the GB´s reef fish community during the TCRMP are related to the presence of the lionfish and the abundance increase of the Nassau grouper (Smith et al. 2018). The first is a story of the arrival of an unwanted guest and the second is a rebuilding stock story of an once abundant commercial fish from this mesophotic ecosystem.

Invasion of the Indo-Pacific Red Lionfish

The invasive Indo-Pacific lionfish was reported the first time at St. Thomas by 2010 (Smith et al. 2018). Since 2011 its abundance and distribution through the USVI has increased. At their peak in the dataset (2015) 112 lionfish were counted on transects at ten sites off the northern USVI, and 15 at seven sites off St. Croix (Figure 15). In 2018 lionfish encounters were lower on northern USVI sites than in 2015, but slightly higher than 2016 and 2017, suggesting a population equilibrium had been reached (Smith et al. 2018).

Figure 14. Grammanik Tiger benthic cover and coral health through time (mean ± SE). a, Coral cover; b, Cover of other benthic community components; c, Prevalence, and extent of bleaching; d, Prevalence of reported diseases; e, Prevalence of old and recent mortality (from Ennis et al. 2019).

Mesophotic sites off both the northern USVIs and St. Croix continue to have the highest abundances of lionfish. The Hind Bank East FSA and Grammanik Tiger FSA especially hold large numbers (Smith et al. 2018).

The preferential habitat for lionfish in the western Atlantic has not been reported empirically; however, based on dives conducted across the USVI shelves by investigators of UVI as well as reports from fishermen it appears that the species utilizes a variety of habitats. Since 2018 investigators of UVI have conducted two types of studies with the lionfish: their mobility (using hydroacoustic technology) and their use of mesophotic habitats. It is expected that these kinds of studies should help understand movement related behavior and habitat/resource use by this invasive fish. Both studies are partially conducted at GB and MCD (Smith et al. 2018).

Figure 15. The abundance (±SEM) of red lionfish on Mesophotic TCRMP transects from 2003 to 2018 (from Smith et al. 2018).

Signs of improvement for the endangered Nassau Grouper

The Nasssau grouper was in the 1960's and 1970's the most common grouper of the USVI reefs. However, their fishery collapsed in the short term in the 1980s due to overfishing, which led to their near-total disappearance south of St. Thomas in the 1980s (Smith et al. 2018). In 2005 the Caribbean Fisheries Management Council closed the yellowfin grouper breeding site at Grammanik Bank, inadvertently protecting a small spawning aggregation of Nassau grouper. These fish may have relocated from the extirpated historic Nassau aggregation located a few kilometers to the west (at MCD).

There is evidence that these management measures may be positively affecting both Nassau and yellowfin grouper populations in the US Virgin Islands. The small Nassau grouper aggregation found on the Grammanik Bank appears to be growing in size since its discovery in 2003 (Smith et al. 2018). Nassau grouper aggregate on the site and presumably spawn there shortly after dark in the months of January through April. The bank is closed seasonally to fishing from February 1 to April 30 and is closed to bottom tending gear year-round, thus providing some protection for the aggregating Nassau grouper.

The Nassau grouper have increased in number on the Grammanik Bank during the week after the full moon of January through April since 2002 (Figure 16). In January, February, March, and April of 2018, between 200 and 360 fish were observed on single dives on the western end of the bank. Numbers in January, February and March were again close to 400. This represents an over 200% increase from the number of

fish observed during the early and mid-2000’s (Smith et al. 2018). In 2019 nearly 300 fish were seen in single dives. Bad weather did not allow for daily surveys however in late afternoon dives fish were seen in spawning coloration (dark and bicolor) and spawning behaviors such as chasing, leading and nuzzling were observed. Spawning rushes and actual gamete release continue to evade the researchers; however, it appears that spawning at some level is occurring, probably after dark. Nassau grouper movement is being studied by researchers at UVI using hydroacoustic telemetry. Fish tagged with VEMCO transmitters are tracked as they utilize the spawning area on the bank, as well as when and how they move and migrate in and out of the closed area.

Furthermore, over 2015 to 2017 there have been reports by divers of the both groupers being seen commonly on reefs around the territory, and fishermen continue to report regular occurrences of Nassau grouper in their fish traps (Smith et al. 2018). In TCRMP survey data from 2015, 2016, and 2017, substantially more Nassau groupers were observed than in earlier years, and they were observed on more sites, including nearshore sites (Figure 17). Additionally, juvenile young-of-the-year Nassau were commonly seen in nearshore areas of St. Thomas and St. John in 2006, 2014, 2015, and 2016 (R. Nemeth, unpub data).

Figure 16. Nassau grouper observed across all northern USVI sites on belt transects, conducted annually from 2003-2017 (from Smith et al. 2018).

The early and tentative recovery of the Nassau grouper in the northern USVI is positive but is far from complete. While fisheries closures have helped, targeted conservation actions may also be important for locking in and building on these gains for this threatened fish (Smith et al. 2018). Nassau grouper caught incidentally from deeper water (>20m deep) usually need to have their swim bladders deflated to allow them to submerge and survive when released. Thus, avoiding incidental capture even with release is important. In the northern USVI, a more complete fishing closure of the Grammanik Bank that encompasses

the full seasonal cycle of Nassau grouper spawning activities (December to May) would ensure minimal incidental capture (Smith et al. 2018). Additionally, creating a migratory corridor between the nearby Hind Bank Marine Conservation District, a no-take closure that appears to support a relatively high adult population on Nassau, would also limit fisheries impacts. Throughout the USVI, more education on Nassau grouper and their protected status would be very helpful. The early life cycle of Nassau grouper typically involves settling in shallow, nearshore structures surrounded by seagrass. Even as populations increase, these juveniles are highly vulnerable to recreation line fishing and spearfishing before they migrate to offshore locations. Education and citizen science opportunities to get the community behind the recovery of Nassau would greatly enhance the protections already in place by encouraging compliance.

Figure 17. Nassau grouper observed across all 19 northern TCRMP sites on belt transects conducted annually from 2003-2018. Note that individual fish may have been counted multiple times across observers at some locations in 2018 (from Smith et al. 2018).

5.4 Reported species within GB The TCRMP at the Grammanik Tiger site has reported around 50 species/groups of stony corals and other benthic groups. The most abundant benthic species are the stony corals Orbicella franksii, O. faveolata and Agaricia lamarcki. Table 11 shows the most representative benthic species and groups.

Table 11. Most representative benthic species recorded by the TCRMP at Grammanik Tiger site. Species/Groups Type Species/Groups Type Agaricia agaricites Scleractinian Scolymia cubensis Scleractinian Agaricia grahamae Scleractinian Stephanocoenia intercepta Scleractinian Agaricia humilis Scleractinian Siderastrea siderea Scleractinian Agaricia lamarcki 3 Scleractinian Millepora alcicornis Hydrocoral Agaricia undata Scleractinian Erythropodium caribaeorum Octocoral Colpophyllia natans Scleractinian Sea Fan Octocoral Diploria labyrinthiformis Scleractinian Clionia delitrix Sponge Dichocoenia stokesii Scleractinian Encrusting sponge Sponge Eusmilia fastigiata Scleractinian Sponge Sponge Montastraea cavernosa Scleractinian Macroalgae Macroalgae Madracis decactis Scleractinian Cladophora spp. Macroalgae Madracis mirabilis Scleractinian Dictyota spp. ** Macroalgae Mycetophyllia ferox Scleractinian Lobophora variegata * Macroalgae Orbicella faveolata 2 Scleractinian Peyssonellia spp. ** Calcareous Macroalgae Orbicella franksii 1 Scleractinian Coralline algae ** Calcareous Porites astreoides Scleractinian Turf algae * Turf Porites porites Scleractinian Filamentous cyanobacteria ** Cyanobacteria Numbers 1, 2 and 3 show the three most abundant stony corals in descending order; * and ** show species/groups other than stony corals with relatively high and intermediate cover values. The names of the species were obtained by analyzing data from the TCRMP.

Regarding the fish community, TCRMP at Grammanik Tiger site has reported 110 species. Table 12 shows the commercially important fish species found at this site; i.e.: name (scientific and common), fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005), conservation status according to the IUCN red list and trophic group according to Ennis et al. 2019. In the case of CFMC’s FMU, only those categories that include the largest and/or most important fish from the commercial point of view have been included in this table. The commercially important species registered at Grammanik Tiger are large groupers (Nassau, yellowfin, yellowmouth, and tiger groupers) and snappers (cubera and schoolmaster snapper), some of them with any degree of threat.

Table 13 shows information of interest of other representative fish species found at this site; i.e.: name (scientific and common) and fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005). In this group of species, the presence of porgies, squirrelfish, grunts, sharks, great barracuda, and lionfish stands out. The first three groups are considered in the CFCM’s FMU. In addition, sharks are common, and lionfish have become a frequent and relatively

abundant inhabitant in the Bank since their first record in 2011. Note that fish censuses on which these conclusions are based are conducted during November and December of each year, outside of the known reproductive aggregation seasons for groupers, snappers, and other commercially important species at the USVI.

Table 12. Commercially important fish species recorded by the TCRMP at Grammanik Tiger site. UICN Red List Trophic Scientific Name1 Common Name1 Fisheries2 Status3 Group1 Cephalopholis cruentata Graysby Groupers Least Concern Piscivore Cephalopholis fulva Coney Groupers Least Concern Invertivore Epinephelus guttatus Red hind Groupers Least Concern Invertivore Epinephelus striatus Nassau grouper Groupers Critically Endangered Piscivore Mycteroperca interstitialis Yellowmouth grouper Groupers Vulnerable Piscivore Mycteroperca tigris Tiger grouper Groupers Data Deficient Piscivore Mycteroperca venenosa Yellowfin grouper Groupers Near Threatened Piscivore Paranthias furcifer Creolefish Groupers Least Concern Planktivore Lutjanus analis Mutton snapper Snappers Near Threatened Piscivore Lutjanus apodus Schoolmaster Snappers Least Concern Piscivore Lutjanus cyanopterus Cubera snapper Snappers Vulnerable Piscivore Lutjanus jocu Dog snapper Snappers Data Deficient Piscivore Lutjanus mahogani Mahogany snapper Snappers Least Concern Piscivore Lutjanus synagris Lane snapper Snappers Near Threatened Piscivore Ocyurus chrysurus Yellowtail snapper Snappers Data Deficient Planktivore Caranx crysos Blue runner Jacks Least Concern Piscivore Caranx latus Horse eye jack Jacks Least Concern Piscivore Caranx lugubris Black jack Jacks Least Concern Piscivore Caranx ruber Bar jack Jacks Least Concern Piscivore Seriola dumerili Greater amberjack Jacks Least Concern Piscivore Seriola rivoliana Almaco jack Jacks Least Concern Piscivore Balistes vetula Queen trigger Triggerfish Near Threatened Invertivore Canthidermis sufflamen Ocean trigger Triggerfish Least Concern Planktivore Calamus calamus Saucereye porgy Porgies Least Concern Invertivore Calamus pennatula Pluma porgy Porgies Least Concern Invertivore Holacanthus ciliaris Queen angel Angelfish Least Concern Invertivore Pomacanthus arcuatus Gray angel Angelfish Least Concern Spongivore Pomacanthus paru French angel Angelfish Least Concern Invertivore Scarus taeniopterus Princess parrotfish Parrotfishes Least Concern Herbivore Sparisoma aurofrenatum Redband parrotfish Parrotfishes Least Concern Herbivore Sparisoma viride Stoplight parrotfish Parrotfishes Least Concern Herbivore 1 From Ennis et al. 2019; 2 According to CFMC 2005; 3 According to UICN Red List Status

Table 13. Other fish species recorded by the TCRMP at the Grammanik Tiger site. Scientific Name1 Common Name1 Fisheries2 Cantherhines macrocerus Whitespotted filefish Triggerfish Melichthys niger Black durgon Triggerfish Xanthichthys ringens Sargassum triggerfish Triggerfish Mulloidichthys martinicus Yellow goatfish Goatfish Mulloidichthys martinicus Yellow goatfish Goatfish Pseudupeneus maculatus Spotted goatfish Goatfish Anisotremus surinamensis Black margate Grunt Anisotremus virginicus Porkfish Grunt Haemulon flavolineatum French grunt Grunt Haemulon plumierii White grunt Grunt Haemulon sciurus Bluestriped grunt Grunt Holocentrus adscensionis Squirrelfish Squirrelfish Holocentrus rufus Longspine squirrelfish Squirrelfish Myripristis jacobus Blackbar soldierfish Squirrelfish Holocentrus rufus Longspine squirrelfish Squirrelfish Myripristis jacobus Blackbar soldierfish Squirrelfish Acanthurus bahianus Ocean surgeonfish Surgeonfish Acanthurus chirurgus Doctorfish Surgeonfish Acanthurus coeruleus Blue tang Surgeonfish Bodianus rufus Spanish hogfish Wrasses Lachnolaimus maximus Hogfish Wrasses Pterois volitans Lionfish - Sphyraena barracuda Great barracuda - Carcharhinus leucas Bull shark - Carcharhinus perezi Caribbean reef shark - Ginglymostoma cirratum Nurse shark - Galeocerdo cuvier tiger shark - Negaprion brevirostris Lemon shark -

1 From Ennis et al. 2019; 2 According to CFMC 2005.

5.5 Primary scientific studies that have or are taking place within GB The scientific studies that have been conducted within GB that may be related with the performance of marine reserves have described and monitored the behavior over time of fish species that use these reserves as sites of spawning aggregation. To this end, these studies had used different and novel technologies. The most recent studies carried out at GB on these matters and their main findings are summarized below.

Kadison et al. 2010 presented the preliminary findings on changes in the Nassau grouper (Epinephelus striatus) population aggregating on the GB since the CFMC protective measures were implemented, based on monitoring from 2004 through 2009. Visual fish surveys by divers using technical NITROX or closed circuit rebreathers were conducted around the full moon each year from January through April, 2004 through 2009. Surveys generally were conducted over 2 to 11 days, beginning the day of the full moon until the new moon, timed to document the arrival and departure of fish. Some groupers were collected daily during the same time period each year. Captured Nassau groupers were measured, sexed using a portable field ultrasound, and tagged. The fish were released close to the collection site using a release cage that could be opened remotely when it reached the sea floor. Spawning population changes from 2004 through 2009 were compared using the number of fish observed in underwater surveys and population characteristics including sex ratio and mean size of fish collected over five years of monitoring. Surveys and trap catches revealed that Nassau aggregated mainly on the GB in February, March and April. They arrived on and around the full moon, peaked in number from 2 - 8 days after the full moon, and departed from 10 to 12 days after the full moon. Fish exhibited courting and spawning colorations typical of spawning time but not observed actually spawning. Spawning occurred under poor light conditions after the divers left the water. Spatially, Nassau groupers were patchily mixed across the reef with yellowfin grouper. The number of Nassau groupers observed in visual surveys increased slowly from 2005 (0-30) through 2007 (5-35) but was higher in 2008 and especially 2009 (40-110). The mean size of Nassau grouper collected in 2004 and 2005 was not significantly different, however it was significantly smaller than in subsequent years. Mean fish size did not significantly change from 2006 through 2009. Although small in terms of number of fish the GB aggregation appears to be slowly rebuilding from the over-exploitation of previous years. In addition, the presence of younger cohorts on the aggregation site in 2009 suggest the possibility of continuity and perhaps the rebounding of a healthy Nassau grouper spawning aggregation. The study showed that the population of the Nassau grouper was apparently recovering and spawning at GB, which makes this site the only known remaining spawning site to this species in USVI.

Kadison et al. 2011 examined yellowfin grouper (Mycteroperca venenosa) patterns of spawning from 2005 - 2010 on the GB. Visual fish surveys by divers using technical NITROX or closed circuit rebreathers were conducted around the full moon each year from February through May, 2005 through 2009. Surveys generally were conducted over 2 to 9 days, beginning the day of the full moon until the new moon, timed to document the arrival and departure of fish. Some groupers were collected daily during the same time period, as well from February through April, 2010. Captured yellowfin groupers were measured, sexed using a portable field ultrasound or by squeezing the abdomen for milt, and tagged. The fish were released close to the collection site using a release cage that could be opened remotely when it reached the sea floor. A subset of female yellowfin groupers was sacrificed in 2006, 2009 and 2010, to determine gonadosomatic indices (GSIs) and to examine histologically. Water temperature 1 m from the sea bottom was recorded hourly from February 2005 through October 2010 at a spot within the core aggregation site. The visual surveys conducted between 2005 and 2009 confirmed that the fish aggregated between February and April each year, with the majority of fish spawning in March and April. Mean hourly water temperature during the spawning season varied between 25.2°C and 27.0°C. The arrival, spawning, and departure of fish coincided each month with a consistent moon phase. All male fish collected on the aggregation site were ripe. Analysis of individual female gonadosomatic indices (GSI) indicated a spawning frequency for most females of 2 - 3 days. Spawning was observed several days in March and April of 2008 and 2009, from 6 through 10 days after full moon. It occurred from four minutes before sunset to at least 20 minutes after,

and probably into the night. The yellowfin grouper spawning aggregation appears fairly intact on the GB, with relatively high numbers of fish and frequent observed spawning but little is known of the historic population size or how spawning behaviour may have changed over time due to changes in population parameters. The combined effect of the seasonal closure of the GB, the 22-year closure of the nearest MCD and the seasonal ban on harvest or sale of yellowfin grouper, has undoubtedly played a key role in maintaining the spawning population that currently exists on the bank. This demonstrates how effective management measures can provide protection and sustainability for aggregation sites. Since few other large spawning aggregations of yellowfin grouper are known to exist in the eastern Caribbean, continued management and protection of the bank is essential.

Schärer-Umpierre et al. (2012b) described sound production by Nassau grouper (Epinephelus striatus) from four different spawning aggregation sites in the Caribbean (BS, Grammnik Bank and Red Hind Marine Conservation District were included in this study). Primary findings were presented in section 4.6

Nemeth and Kadison 2013 presented the first report of the aggregation and mass spawning of the Bermuda chub (Kyphosus sectatrix) on GB. Underwater visual surveys using technical Nitrox and closed circuit rebreathers were conducted from December 2002 to March 2013 and documented spatial and temporal patterns of movement and aggregation formation along this mesophotic reef. Spawning coloration and gamete release of the Bermuda chub were observed and filmed. The largest aggregations of this species were observed from January to March from 0 to 11 days after the full moon. Reproductive aggregation of K. sectatrix coincided with the spawning season of Nassau (Epinephelus striatus) and yellowfin (Mycteroperca venenosa) groupers. These spatial and temporal patterns of reproductive aggregation and spawning suggest that K. sectatrix, an herbivore, may also be a transient aggregating species. Color patterns and behaviors associated with aggregation and spawning were described and compared to spawning characteristics observed in other species. The two individuals collected on the GB had full stomachs of Lobophora variegata, which occurs in relative abundance in deep places of this bank. In the future, the key ecological role of these fish in this ecosystem should be studied.

Jackson et al. (2014) studied the Nassau grouper (Epinephelus striatus) genetic connectivity across the Caribbean basin, including samples from Grammanik Bank and Bajo de Sico. All samples were genotyped for two mitochondrial markers and nine microsatellite loci, and a subset of the samples was genotyped for

4,234 SNPs. Authors found genetic differentiation across the Caribbean using mtDNA (FST = 0.206, p<0.001), microsatellites (FST = 0.002, p = 0.004) and SNPs (FST = 0.002, p = 0.014), and identified three potential barriers to larval dispersal. The identified genetically isolated regions mirrored those seen for other invertebrate and fish species in the Caribbean basin. Other primary findings were presented in section 4.6.

Rowell et al. 2015 used passive acoustic and acoustic telemetry methods to determine temporal patterns of reproductive activity, site usage, and fish movements of Nassau grouper (Epinephelus striatus) and yellowfin grouper (Mycteroperca venenosa) in order to assess the effectiveness of current management strategies at two adjacent marine protected areas (MPAs): Grammanik Bank (GB) and Hind Bank Marine Conservation District (MCD). This was done taking advantage of the fact that the two species produce sounds associated with reproductive behavior (courtship-associated sounds, CAS). Passive acoustic studies were conducted using DSG-Ocean long-term acoustic recorders deployed at 2 fixed locations within the GB and MCD prior to Nassau and yellowfin grouper spawning seasons in 2011 and 2012. Ultrasonic telemetry data were analyzed from a separate previous fish tracking study carried out from 2007 to 2012.

Patterns of sound production and ultrasonic acoustic tag detections showed that both species formed spawning aggregations from January through May at the GB, highlighting the current seasonal regulations (1 February to 30 April) as insufficient for protecting spawning stocks during the entire reproductive season. Acoustic tagging confirmed connectivity between the GB and MCD and exposed the broad extent of habitat used, including non-protected areas, during the spawning season. Spawning did not likely occur within the MCD, but the MPA did support abundances of calling individuals during spawning periods, indicating that both species produce CAS away from their spawning sites. This finding coupled with the detection of routine migrations between spawning and non-spawning sites presents a potential mechanism to lead conspecifics to the aggregation site and thereby increase reproductive fitness and spawning output. A continuation and expansion of passive acoustic and ultrasonic telemetry monitoring will be important to define the range of essential reproductive and migratory habitat for Nassau and yellowfin groupers and determine whether the current geographic limits of the GB and MCD should be expanded or modified to ensure the complete protection of spawning stocks, which may be necessary for full recovery and maintenance of these aggregations. The current 3 mo (February through April) GB area and yellowfin grouper fishery closures do not encompass the more extensive spawning period documented for either species in this study and therefore do not prevent incidental catch mortalities outside of the protected areas or season.

Biggs and Nemeth (2016) utilized acoustic transmitters and a receiver array to track dog snapper (Lutjanus jocu) and Cubera snapper (Lutjanus cyanopterus) within a multi-species spawning aggregation site at the Grammanik Bank from June 2014 to September 2015. Acoustic detections showed that both species utilized spawning areas of 1.4 to 1.5 km2, centered at the shelf promontory. The aggregation area of L. cyanopterus was situated along the shelf edge; the L. jocu aggregation may have been displaced by L. cyanopterus as it occupied some of the inner shelf as well. Receivers along the shelf edge recorded the longest residence times during the hours of spawning (16:45 to 20:00 h), suggesting this is likely a spawning site for both species. L. cyanopterus aggregated monthly from May through November, with residence time peaking in August. L. jocu aggregated monthly throughout the year and residence time did not vary significantly by month. Each month, detections increased in the week before and the first week after the full moon, but then decreased to zero by the third week after the full moon. This study outlines the spatial and temporal dimensions of the spawning aggregation, which can be applied to the management and development of protected areas.

Bernard et al. 2016 studied some aspects of population genetic dynamics of the Nassau grouper (Epinephelus striatus) at two localities in the Greater Caribbean: Cayman Island and USVI (site at GB). The authors addressed two objectives: to explore which factors (i.e., local vs. external recruitment) might be key in shaping the Nassau grouper USVI FSA population recovery; and examined the consequences of severe past overfishing on this FSA’s current genetic status. They genotyped individuals (15 microsatellites) from the USVI FSA comprising three successive spawning years (2008–2010), as well as individuals from a much larger, presumably less impacted, Nassau grouper FSA in the Cayman Islands, to assess their comparative population dynamics. No population structure was detected between the USVI and Cayman FSAs (FST = −0.0004); however, a temporally waning, genetic bottleneck signal was detected in the USVI FSA. Parentage analysis failed to identify any parent–offspring matches between USVI FSA adults and nearby juveniles, and relatedness analysis showed low levels of genetic relatedness among USVI FSA individuals. Genetic diversity across USVI FSA temporal collections was relatively high, and no marked differences were found between the USVI and Cayman FSAs. These collective results suggest that

external recruitment is an important driver of the USVI FSA recovery. Furthermore, despite an apparent genetic bottleneck, the genetic diversity of USVI Nassau grouper has not been severely compromised. Our findings also provide a baseline for future genetic monitoring of the nascent USVI aggregation.

Jossart et al. (2017) examined environmental factors that influence detection variability on a mesophotic coral reef south of St. Thomas (GB and MCD). Data from a stationary transmitter were examined against numerous environmental variables from June to September 2011. A generalized linear model was used to examine the daily detection proportion response to eight different environmental variables. Factors which had strong negative effects on detections received included when the current direction was flowing from receiver to transmitter, current speeds above 0.2 ms−1, a strong temperature gradient between transmitter and receiver, and increased water temperature. Detections varied throughout the different time periods of the day with sunset and sunrise having significantly lower detections than day, and sunset having significantly lower detections than night. The results highlight the importance of conducting a long-term range test and will aid design of future passive acoustic telemetry studies on mesophotic coral reefs.

Kadison et al. (2017) used two long-term fisheries independent datasets, collected by the U.S. Virgin Islands Territorial Coral Reef Monitoring Program and the National Oceanographic and Atmospheric Administration Center for Coastal Monitoring and Assessment, to compare both the occurrence and size of several species of large and commercially important reef fishes between the northern USVI St. Thomas and St. John) and St. Croix. These fishes are primarily apex piscivores and generally the first species overexploited in small-scale fisheries. The disparities between the fish communities on the two island shelves cannot be explained solely by differences in habitat (coral cover, rugosity) or fisheries management, such as the relative amount of marine protected area in local waters. They are instead caused by a combination of other interrelated factors including water depth, fishing methodology, fishable area, and the presence or absence of viable fish spawning areas. The authors discuss the possible positive effect that the two southern St. Thomas reserves (GB and MCD) are so close together and surrounded by a wide island shelf, while the St Croix reserves are more isolated from each other and are surrounded by a narrower island platform. The authors suggest that St. Croix is an example of a severely overfished Caribbean island, and this study illustrates the need for management of artisanal fisheries that is tailored to the physical and spatial constraints imposed by shallow insular platforms.

Rowell et al. (2018) identified a new sound produced by Nassau Grouper (Epinephelus striatus) in association with, although potentially not exclusive to, an agonistic interaction at a spawning aggregation. A synchronous audio—video recorder was deployed at BS at a depth of 50 m. This sound was compared with an unidentified ambient sound previously recorded at GB in 2011. The two sounds matched and allowed the authors to establish that they were produced by the same species of grouper. The authors also provided a behavioral and acoustic description for identification of this sound in future studies. The discovery of a third type of sound produced by Nassau Grouper further highlights the importance of acoustic communication coupled with visual displays in fishes, and enhances our ability to decipher patterns of different behaviors. Furthermore, identification of a new sound increases the ability to document the presence of this endangered species at spawning sites. Future efforts may reveal that the sound is produced within additional behavioral contexts during and outside of spawning seasons, such as the defense of territories or food resources. Continued efforts to catalogue the sounds and behaviors of species like Nassau Grouper will increase our ability to monitor and understand fish behaviors.

Cherubin et al. (2020) presented a new persistent robotic approach to conduct Passive Acoustic Monitoring (PAM) surveys and its application to the study of grouper FSA dynamics. The experimental phase was conducted at GB and Red Hind Marine Conservation District. To facilitate fish call detections, the authors developed an algorithm based on machine learning and voice recognition methods to identify and classify the sounds known to be produced by certain species during FSA. This algorithm currently operates on a SV3 Liquid Robotics wave glider, an autonomous surface vehicle which has been fitted to accommodate a passive acoustic listening device and can cover large areas under a wide range of sea conditions. Fish sounds detections, classification results, and locations along with environmental data are transmitted in real-time enabling verification of the sites with high detections by divers or other in situ methods. Recent surveys in the US Virgin Islands with the SV3 Wave Glider are revealing for the first time the spatial and temporal distribution of fish calls surrounding known FSA sites. These findings are critical to understanding the dynamics of fish populations because calling fish were detected several kilometers away from the known FSAs. These courtship associated sounds from surrounding areas suggest that other FSAs may exist in the region.

Nemeth et al. 2020 assessed the yellowfin grouper (Mycteroperca venenosa) reproductive characteristics, movement patterns and courtship behaviors associated at GB, between 2004 and 2014. The aim of this study was to (1) document the spatial and temporal patterns of M. venenosa around the GB FSA (fish spawning aggregation), (2) examine changes in annual spawning population characteristics (length frequency, sex ratios), (3) examine the reproductive biology of females through histological analysis, and (4) describe and quantify M. venenosa spawning behavior and coloration patterns. Underwater visual counts of groupers on the GB were made from December 2002 to August 2014. The UVC were conducted on technical NITROX (2002–2007) or closed circuit rebreathers (2008–2014) using a variety of techniques. Some groupers were collected between March 2004 and April 2010. Captured yellowfin groupers were measured, sexed using a portable field ultrasound or by squeezing the abdomen for milt, and tagged. The fish were released close to the collection site using a release cage that could be opened remotely when it reached the sea floor. A subset of female yellowfin groupers captured 2–12 days after full moon during March and April in 2006, 2007, 2009 and 2010, were sacrificed (or had died) to examine their reproductive biology. Fish arrived at the FSA site around full moon and departed 10–12 days after full moon (dafm), during two or three consecutive months, from January to May each year. Males were significantly larger than females and preceded females at the spawning site. Courtship coloration and behaviors showed distinct patterns relative to lunar date and time of day. Spawning was observed for several days each month in 2008, 2009, 2011 and 2014, from 6 to 10 dafm. Female gonadosomatic index (GSI) values were highest from 4 to 7 dafm. Spawning, which began at sunset, consisted of 7 to 12 males following one female along the bottom before ascending 10–20 m, then “rushing” upward to release gametes. Histological analysis of ovaries indicated females spawned every 2–3 nights, although 11.6% were capable of spawning two consecutive nights. Total spawning population size of yellowfin grouper fluctuated from 600 to 1100 fish during the study period. Based on size-frequency analysis and other metrics, the M. venenosa spawning population at the GB appears to be stable at this time with existing regulations.

6. Hind Bank Marine Conservation District (MCD)

6.1 History and description of MCD Hind Bank Marine Conservation District (Seasonal Fishing Closure Area) was initially designated by NOAA in 1990 as an area of approximately 14 square nautical miles in the EEZ southwest of St. Thomas, U.S. Virgin Islands to manage red hind spawning aggregations (Epinephelus guttatus). Initially, the closure runs from December 1 through February 28 each year (Federal Register 1990). In 1999, this area was declared a year-round no-take area and called Red Hind Marine Conservation District. This was a consequence of a cooperative effort between the CFMC and local fishers to protect deep coral reefs and improve fishery resources (Federal Register 1999). MCD has a total area of 44.6 km2 and is located in the EEZ at 18°13.2’N 65°06.0’ W; 18°13.2’ N 64°59.0’ W, and 18°11.8’ N 64°59.0’ W; 18°10.7’ N 65°06.0’ W (Federal Register 1990) (Figure 18). The no-take area is also 44.6 km2. MCD is governed by the Caribbean Fisheries Management Council (CFMC), The National Oceanographic and Atmospheric Agency (NOAA), and the Virgin Islands Department of Natural Resources (VI-DPNR). MCD is a year round no- take zone (Pittman et al. 2014, Schärer-Umpierre et al. 2014). Within the MCD is a known red hind Epinephelus guttatus FSA site (Nemeth 2005). Regulations enacted at this MPA have resulted in increases in fish size, numbers, and landings of red hind (Nemeth 2005). The MCD also supports an FSA of tiger grouper Mycteroperca tigris but not Nassau or yellowfin grouper.

Figure 18. Location of the Hind Bank Marine Conservation District (MCD).

6.2 Marine ecosystems present in MCD

The MCD is located southwest of St Thomas on the border of the Puerto Rican shelf (Fig 18). The benthic composition of the MCD (44.6 km2) includes consolidated and unconsolidated habitats (Fig 19) at depths of 30 to 60 m (Smith et al. 2010). Two-thirds of the MCD is covered by dense coral reefs (coral cover = 24.1%) dominated by Orbicella spp. (formerly Montastraea spp.). Among the consolidated habitats there are extensive mesophotic coral reefs and colonized hard bottoms (pavements). The coral reefs are morphologically diverse with primary, secondary, and tertiary high banks (35.8% of the MCD). It also has patch/low banks, hardground flat bottoms (18%), and rugose hillock basins (6.5%) containing thousands of coral knolls (2-10 m high). Among the unconsolidated habitats, there are sand channels and algal plains (Smith et al. 2010). Figure 19 shows the distribution of these habitats across the MCD.

Fig 19. Habitats within the Hind Bank Marine Conservation District, St. Thomas, USVI (from Smith et al. 2010).

6.3 Condition and changes through time of marine ecosystems within MCD TCRMP run by scientists of the UVI has two permanent sampling sites at MCD. These sampling spots are named “College Shoal East” and “Hind Bank East FSA”. The first site, 30 m depth, is located at 18,18568 N and -65,07677 W, and the second, 39 m depth, is located at 18.20217 N and -65.00158 W (Ennis et al. 2019). Both sites had been monitored since 2003, with permanent transects installed in 2007. Changes in benthic community structure, coral health, and reef fish have been documented since then. The main documented changes are summarized below.

According to the 2019 TCRMP report (Ennis et al. 2019), the condition of marine ecosystems at both sites in the MCD can be summarized by the decrease since 2012-2013 in coral cover of Orbicella (the most abundant coral). The likely reason for this coral cover decrease is the higher prevalence of white diseases. Additionally, during this same period of time, macroalgae cover has maintained an upward trend.

The prevalence and extent of bleaching at TCRMP sites are shown in figure 13. At the College Shoal East site, the 2005 event was the strongest, with a prevalence near 50% and an extent higher than 90%. At this site, the 2019 bleaching event had a prevalence near 45% and an extent less than 15%. At the Hind Bank East site, the 2005 event produced a prevalence near 10% and an extent close to 20%. At this site, the 2019 bleaching event had a prevalence higher than 30% and an extent close to 15% (Ennis et al., 2019).

According to Ennis et al. (2019) the main threats at the College Shoal East site are i) Coral white diseases at chronically high levels (> 1% prevalence). ii) High abundance of the invasive Indo-Pacific Lionfish (Pterois volitans). The main threats to the Hind Bank East site are i) Susceptibility to chronic coral white diseases. ii) Periodic disease outbreaks follow high thermal stress. iii) High abundance of the Indo-Pacific lionfish (Pterois volitans), which is affecting juvenile native fish populations.

6.3.1 Benthic community structure Hind Bank site.- The site is dominated by boulder star corals (Orbicella spp.) with a high abundance of lettuce corals (Agaricia spp.). The 2005 bleaching event initially decreased coral cover by 21.8% but since then 71.4% of the lost coral cover has been regained (fig. 20a). The appearance of SCTLD in 2019 has accelerated coral cover decline. The algal community is co-dominated by epilithic algae and the macroalgae Lobophora variegata. Since 2013 macroalgae cover has been increasing (fig. 20b) (Ennis et al., 2019).

College Shoal site.- The site is among the TCRMP sites with the highest coral cover (38.2% in 2011) and is dominated by the boulder star coral (Orbicella spp.). This site lost 10.1% of its coral cover after the 2005 bleaching event (fig. 20c) and coral cover has been declining ever since 2012. SCTLD arrived at this site in 2019 and has accelerated the decline of coral cover. The algal community is dominated by the macroalgae Lobophora variegata and lesser proportion by epilithic algae. Since 2014 macroalgae cover has been increasing (fig. 20d) (Ennis et al. (2019).

6.3.2 Coral Health Hind bank site.- Unlike other US Caribbean sites, bleaching has not been detected as a major factor. Bleaching during 2005 was underestimated because sampling occurred before the peak in heat stress. Neither the 2010 or 2019 events were detected during sampling. In later years (Figure 21a), low colony extent bleaching was often associated with granular bleaching. This bleaching pattern shows pigmented spots surrounded by bleached tissue (Ennis et al. 2019). Coral diseases are common at the Hind Bank and may be increasing. Figure 21b shows disease prevalence. White disease was the dominant disease, and in 2011 showed a peak of incidence. In 2009, there was a high prevalence of intercostal mortality syndrome, which is only known from mesophotic coral reefs (Smith et al. 2010b). SCTLD had begun to impact the site since 2019. Partial mortality increased after the 2005 bleaching event and the high prevalence was not reduced until 2011. Recent partial mortality is high and reflects the impacts of disease and predation. Figure 21c shows old and recent mortality prevalence.

College Shoal site.- Figure 21d shows bleaching prevalence and bleaching extent. The 2005 bleaching event had a low prevalence, although corals that bleached tended to lose color over their entire surface. The 2010 coral bleaching event had no apparent effect above background bleaching levels. Bleaching in years without thermal stress tends to be moderate. Diseases were dominated by white disease, which reached very high prevalence after the 2005 bleaching event, with an outbreak that lasted for two years in 2006 and 2007.

This disease was again very prevalent in 2011 after the 2010 bleaching event, even without apparent thermal bleaching. The impacts of SCTLD were very severe in 2019, with about 25% of colonies displaying disease signs that were likely related. Figure 21e shows disease prevalence. Old partial mortality was elevated on corals after the mortality from the 2005 bleaching event, and this level has remained stable through 2011. Recent partial mortality is always relatively high, much of it attributable to fish bites. Figure 21f shows old and recent mortality prevalence (Ennis et al. 2019).

Figure 20. MCD benthic cover through time (mean ± SE). a, Hind Bank East site coral cover; b, Hind Bank East site cover of other benthic community components; c, College Shoal East site coral cover; b, College Shoal East site cover of other benthic community components (from Ennis et al. 2019).

6.3.3 Reef fish

The “Hind Bank” monitoring site (a TCRMP site) hosts a multispecies spawning aggregation, including a recovering population of the commercially important red hind grouper (Epinephelus guttatus). Data from early 2000s and later during the TCRMP have corroborated the rebuilding of the red hind’s population at this site (Nemeth 2005, Ennis et al. 2019).

Figure 21. MCD coral health through time (mean ± SE). a, Hind Bank East site prevalence and extent of bleaching; b, Hind Bank East site prevalence of reported diseases; c, Hind Bank East site prevalence of old and recent mortality; d, College Shoal East site prevalence and extent of bleaching; e, College Shoal East site prevalence of reported diseases; f, College Shoal East site prevalence of old and recent mortality (from Ennis et al. 2019).

6.4 Reported species within MCD TCRMP has two sampling points within MCD (College Shoal East and Hind Bank East). Additionally, in 2006 and 2008, two studies characterized this Marine Managed Area (Armstrong et al. 2006, Nemeth et al. 2008). The results from these studies about variation in benthic species and reef fish are summarized below.

There are 74 species/taxonomic groups of benthic algae, sponge, scleractinian corals, hydrocorals, and octocorals reported within MCD (Table 14). The most abundant groups are algal turfs and the macroalgae Lobophora variegata. Among scleractinian corals, the most common are Orbicella spp. and Agaricia spp.

Table 14. Most representative benthic species recorded by the TCRMP, Armstrong et al. 2006, Nemeth et al. 2008 at the MCD. Species/Groups Type Species/Groups Type Agaricia agaricites Scleractinian Siderastrea siderea Scleractinian Agaricia grahamae Scleractinian Millepora alcicornis Hydrocoral Agaricia humilis Scleractinian Ellisella barbadensis Octocoral Agaricia lamarcki 3 Scleractinian Gorgonia sp. Octocoral Agaricia undata Scleractinian Leptogorgia hebes Octocoral Colpophyllia natans Scleractinian Plexaurella nutans Octocoral Diploria labyrinthiformis Scleractinian Pseudoplexaura sp. Octocoral Dichocoenia stokesii Scleractinian Pseudopterogorgia sp. Octocoral Eusmilia fastigiata Scleractinian Agelas clathrodes Sponge Helioseris cucullata Scleractinian Agelas conifera Sponge Madracis decactis Scleractinian Amphimedon compressa Sponge Madracis mirabilis Scleractinian Clionia delitrix Sponge Montastraea cavernosa Scleractinian Geodia neptuni Sponge Mycetophyllia ferox Scleractinian Xestospongia muta Sponge Orbicella faveolata 2 Scleractinian Cladophora spp. Macroalgae Orbicella franksii 1 Scleractinian Dictyota spp. ** Macroalgae Porites astreoides Scleractinian Lobophora variegata * Macroalgae Porites porites Scleractinian Udotea cyathiformis Macroalgae Scolymia cubensis Scleractinian Peyssonellia spp. ** Calcareous Macroalgae Solenastrea bournoni Scleractinian Turf algae * Turf

Stephanocoenia intercepta Scleractinian Filamentous cyanobacteria ** Cyanobacteria Numbers 1, 2 and 3 show the three most abundant stony corals in descending order; * and ** show species/groups other than stony corals with relatively high and intermediate cover values. The names of the species were obtained by analyzing data from the TCRMP in https://sites.google.com/view/usvi-tcrmp-data-archive/home

Table 15. Representative commercially important fish species recorded by the TCRMP, Nemeth et al. 2008 at the MCD. UICN Red List Trophic Scientific Name1 Common Name1 Fisheries2 Status3 Group1 Cephalopholis cruentata Graysby Groupers Least Concern Piscivore Cephalopholis fulva Coney Groupers Least Concern Invertivore Epinephelus guttatus Red hind Groupers Least Concern Invertivore Epinephelus striatus Nassau grouper Groupers Critically Endangered Piscivore Mycteroperca interstitialis Yellowmouth grouper Groupers Vulnerable Piscivore Mycteroperca tigris Tiger grouper Groupers Data Deficient Piscivore Mycteroperca venenosa Yellowfin grouper Groupers Near Threatened Piscivore Paranthias furcifer Creolefish Groupers Least Concern Planktivore Lutjanus analis Mutton snapper Snappers Near Threatened Piscivore Lutjanus apodus Schoolmaster Snappers Least Concern Piscivore Lutjanus buccanella Blackfin snapper Snappers Data Deficient Piscivore Lutjanus cyanopterus Cubera snapper Snappers Vulnerable Piscivore Lutjanus griseus Gray snapper Snappers Least Concern Piscivore Lutjanus jocu Dog snapper Snappers Data Deficient Piscivore Lutjanus mahogani Mahogany snapper Snappers Least Concern Piscivore Lutjanus synagris Lane snapper Snappers Near Threatened Piscivore Ocyurus chrysurus Yellowtail snapper Snappers Data Deficient Planktivore Caranx crysos Blue runner Jacks Least Concern Piscivore Caranx latus Horse eye jack Jacks Least Concern Piscivore Caranx lugubris Black jack Jacks Least Concern Piscivore Caranx ruber Bar jack Jacks Least Concern Piscivore Seriola dumerili Greater amberjack Jacks Least Concern Piscivore Seriola rivoliana Almaco jack Jacks Least Concern Piscivore Balistes vetula Queen trigger Triggerfish Near Threatened Invertivore Canthidermis sufflamen Ocean trigger Triggerfish Least Concern Planktivore Calamus bajonado Jolthead porgy Porgies Least Concern Invertivore Calamus calamus Saucereye porgy Porgies Least Concern Invertivore Holacanthus ciliaris Queen angel Angelfish Least Concern Invertivore Pomacanthus arcuatus Gray angel Angelfish Least Concern Spongivore Pomacanthus paru French angel Angelfish Least Concern Invertivore Scarus guacamaia Rainbow parrotfish Parrotfishes Near Threatened Herbivore Scarus taeniopterus Princess parrotfish Parrotfishes Least Concern Herbivore Sparisoma aurofrenatum Redband parrotfish Parrotfishes Least Concern Herbivore Sparisoma viride Stoplight parrotfish Parrotfishes Least Concern Herbivore 1 From Ennis et al. 2019; 2 According to CFMC 2005; 3 According to UICN Red List Status

The fish community at MCD is composed of 142 species (Tables 15 and 16). Table 15 shows the commercially important fish species with their fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005), conservation status according to the IUCN red list, and trophic group according to Ennis et al. (2019). The commercially important species registered at MCD are groupers (red hind, yellowmouth grouper, tiger grouper, Nassau grouper, yellowfin grouper, coney, graysby) and snappers (schoolmaster, mutton snapper, dog snapper, gray snapper, cubera snapper). Table 16 shows representative fish species found at this site and their fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005). Note that in 2011, the presence of the lionfish was already registered in this Marine Managed Area.

Table 16. Other fish species recorded by the TCRMP at the MCD. Scientific Name1 Common Name1 Fisheries2 Cantherhines macrocerus Whitespotted filefish Triggerfish Melichthys niger Black durgon Triggerfish Xanthichthys ringens Sargassum triggerfish Triggerfish Mulloidichthys martinicus Yellow goatfish Goatfish Mulloidichthys martinicus Yellow goatfish Goatfish Pseudupeneus maculatus Spotted goatfish Goatfish Anisotremus surinamensis Black margate Grunt Anisotremus virginicus Porkfish Grunt Haemulon flavolineatum French grunt Grunt Haemulon plumierii White grunt Grunt Haemulon sciurus Bluestriped grunt Grunt Holocentrus adscensionis Squirrelfish Squirrelfish Holocentrus rufus Longspine squirrelfish Squirrelfish Myripristis jacobus Blackbar soldierfish Squirrelfish Holocentrus rufus Longspine squirrelfish Squirrelfish Myripristis jacobus Blackbar soldierfish Squirrelfish Acanthurus bahianus Ocean surgeonfish Surgeonfish Acanthurus chirurgus Doctorfish Surgeonfish Acanthurus coeruleus Blue tang Surgeonfish Bodianus rufus Spanish hogfish Wrasses Lachnolaimus maximus Hogfish Wrasses Pterois volitans Lionfish - Scomberomorus cavalla King mackerel - Scomberomorus regalis Cero - Sphyraena barracuda Great barracuda - Carcharhinus leucas Bull shark - Carcharhinus perezi Caribbean reef shark - Ginglymostoma cirratum Nurse shark - Galeocerdo cuvier Tiger shark - Negaprion brevirostris Lemon shark - 1 From Ennis et al. 2019; 2 According to CFMC 2005. From Nemeth et al. 2008.

6.5 Primary scientific studies that have or are taking place within MCD The scientific studies that have been conducted within MCD related to the performance of marine reserves have described and monitored the behavior over time of fish species that use these reserves as sites of spawning aggregation. To this end, these studies had used different and novel technologies. The most recent studies carried out at MCD and their main findings are summarized below

Nemeth et al. (2007) compared the spatial and temporal patterns of red hind (Epinephelus guttatus) movement and migration from annual spawning aggregations on St. Thomas (MCD) and St. Croix (Lang Bank). Around ST. Thomas E. guttatus migrated 6–33 km from a functional spawning migration area of 500 km2 and around St. Croix E. guttatus migrated 5–18 km from an area of 90 km2. Similarities between sites were found in regards to timing of movement, temporal and spatial changes in sex ratios, annual and lunar predictability and were synchronized with environmental cues. E. guttatus spawning aggregations in the Virgin Islands occur between the winter solstice (i.e., after December 20) and about February 20 of any year and show a distinctive peak 20–40 days after the winter solstice. Spawning typically occurred during periods of declining seawater temperature and slacking currents within a temperature range of 26–27.5°C and current speed of 2.5–3.5 cm s–1. Males arrived early to spawning sites and stayed longer than females. These gender-based behavioral patterns are important to E. guttatus reproductive dynamics and must be factored into future studies and the design of fisheries regulations to ensure sustainability of spawning aggregation sites. The predictability of E. guttatus spawning aggregations relative to the winter solstice will be extremely beneficial for defining the temporal and spatial aspects of area closures. The consistency and synchrony of movement and migration will improve both the efficiency of planning research and monitoring programs and directing enforcement activities during critical time periods. Applying this knowledge strategically will maximize the limited resources available for research and enforcement and lead to greater protection of spawning aggregations.

Nemeth et al. (2008) investigated what factors influence timing of spawning or selection of aggregation sites in red hind (Epinephelus guttatus) in the eastern Caribbean. The surveys were conducted at MCD, Lang Bank and Saba from December 2005 through February 2006. These data were compared to seven years of previous research on red hind spawning within the USVI. At each site visual counts were conducted using SCUBA to estimate red hind density, the spawning population was sampled daily to determine female gonado-somatic index., and an acoustic Doppler current profiler (ADCP) was deployed during the spawning season to measure current speed and direction and water temperature. Sea water temperature was relatively uniform across the region. Average daily temperature below 25 m declined from 27.5ºC in December to 26.2ºC in February at all sites, and ranged from 26.5ºC to 26.7ºC during the week of the January full moon when fish were spawning. During the spawning season current speeds ranged from 7 to 21 cm s-1 in Saba, 8 to 30 cm s-1 in St. Croix), and 10 to 22 cm s-1 in St. Thomas. During the week of spawning in January, the average current speed near the reef remained the same or slowed and was 10.4 cm s-1 in Saba, 13.1 cm s-1 in St. Croix, and 15.3 cm s-1 in St. Thomas. General current direction the week before spawning was southwest at all sites. A week later, during spawning (i.e., around full moon) average current direction shifted to 260 (west) in St. Thomas, 196 (south-southwest) in St. Croix, and 178 degrees (south) in Saba. In each case the current would carry fertilized eggs and larvae onto the shelf. Data suggest that the location of spawning sites may be influenced by the presence of slower across-shelf currents that maximize retention of eggs and larvae. The authors also found that the majority of red hind within both St. Thomas and St. Croix spawning populations migrated upcurrent to their respective spawning aggregation sites. If eggs and

newly hatched larvae drift slowly down current, they may be in the vicinity of adult home ranges at time of settlement. If this is occurring, then each red hind spawning aggregation may be composed of a distinct subpopulation that is partly self-recruiting. Due to the vulnerability of spawning aggregations and their potential connection to sustaining the local population through self recruitment, it is critical that all spawning aggregation sites are protected from fishing and marine protected area (MPA) boundaries are appropriate for species-specific behavioral patterns. The knowledge that red hind spawning aggregations are extremely limited in space and time can be applied strategically to maximize the limited resources available for research, monitoring and enforcement and lead to more effective MPAs and potentially greater protection of spawning aggregations.

Cherubin et al. (2011) characterized the flow field at MCD, at the shelf break of the insular shelf, for red hind grouper (Epinephelus guttatus) in relation to this species spawning events. Current measurements were profiled throughout the water column for almost a year at the spawning site. The characteristics of the flow field and its evolution after spawning were investigated by using a numerical ocean model that resolved the observed tide and simulated the island scale flow where passive, neutrally buoyant virtual particles were released for 10 days to trace the flow pathways. Observed currents during the spawning period revealed that the flow was vertically sheared, to the south and weakest at the bottom, and to the west or east at the surface. The tidal analysis revealed that the flow at the time of spawning was directed across and on-shelf, although weaker close to the bottom. The model showed that the initial on-shelf transport was counteracted by the bottom flow directed to the shelf break, where virtual particles were entrained by the downwelling flow. A significant percent of particles resided less than two hundred meters deep, in the vicinity of the chlorophyll maximum and returned to the shelf break, close to the release location within 8–10 days. This journey was largely controlled by the timing between downwelling at the spawning site and upwelling further east at the shelf break, which was driven by the coupling between wind and tide induced vertical movements at the shelf break and deeper. The release location, vertical rotation of its flow field, and its transport properties were shown to be relatively resilient to the passage of transient sub-mesoscale eddies as well as to acute mesoscale flow reversals, suggesting that physical retention is maximized in the area surrounding the spawning site.

Ibrahim et al. (2019) proposed a method for the classification of call types of red hind grouper Two distinct call types of red hind were analyzed. The grouper calls were recorded at ALS and MCD. Experimental results showed that the innovative approach produces superior results in comparison with those obtained by non-ensemble methods. The algorithm reliably classified red hind call types with over 90% accuracy and successfully detected some calls missed by human observers.

Kadison et al. (2017) used two long-term fisheries independent datasets, collected by the U.S. Virgin Islands Territorial Coral Reef Monitoring Program and the National Oceanographic and Atmospheric Administration Center for Coastal Monitoring and Assessment, to compare both the occurrence and size of several species of large and commercially important reef fishes between the northern USVI St. Thomas and St. John) and St. Croix. These fishes are primarily apex piscivores and generally the first species overexploited in small-scale fisheries. The disparities between the fish communities on the two island shelves cannot be explained solely by differences in habitat (coral cover, rugosity) or fisheries management, such as the relative amount of marine protected area in local waters. They are instead probably caused by a combination of several other interrelated factors including water depth, fishing methodology, fishable area, and the presence or absence of viable fish spawning areas. The authors discuss the possible positive effect that the two southern St. Thomas reserves (GB and MCD) are so close together and surrounded by a wide island shelf, while the St Croix reserves are more isolated from each other and are surrounded by a narrower island platform. The authors believe that St. Croix may be an example of a severely overfished Caribbean island, and this study illustrates the need for management of artisanal fisheries that is tailored to the physical and spatial constraints imposed by shallow insular platforms.

7. Lang Bank Red Hind Spawning Aggregation Area (LB)

7.1 History and description of LB Lang Bank (red hind spawning aggregation area) was established by NMFS via the MSFC & M Act in 1993 (Federal Register 1993) to improve fisheries management, emphasizing protecting red hind spawning aggregations (Epinephelus guttatus). LB has a total area of 11.7 km2 and is located in the EEZ offshore eastern of St. Croix at A 17°50.2’ N 64°27.9’ W; B 17°50.1’ N 64°26.1’ W; C 17°49.2’ N 64°25.8’ W; D 17°48.6’ N 64°25.8’ W; E 17°48.1’ N 64°26.1’ W; F 17°47.5’ N 64°26.9’ W (Fig. 22). The no-take area is 11.7 km2. LB is governed by the Caribbean Fisheries Management Council (CFMC), The National Oceanographic and Atmospheric Agency (NOAA), and the Virgin Islands Department of Natural Resources (VI-DPNR). MCD is a seasonal no-take zone between December 1 to February 28 (Pittman et al. 2014, Schärer-Umpierre et al. 2014).

Figure 22. Location of the Lang Bank Red Hind Spawning Aggregation Area (LB)

7.2 Marine ecosystems present in LB LB is a submerged coral reef system located along the north-eastern shelf of St. Croix, USVI. LB is an offshore MCE (Ennis et al., 2019). At 30-50 m depth, there are five benthic habitats, including a Bank Coral Reef system, Colonized Pavement, Colonized Rhodolith Reef, Spur, and Groove Reef, and Patch Reef (Fig. 23). The Bank Coral Reef habitat occupied an estimated ~32% of the total area surveyed. It is a massive continuous formation of scleractinian corals, particularly boulder star corals (Orbicella franksii) throughout the deep outer shelf basin of the bank, with an average live coral cover of 29%. The Colonized Pavement was the most extensive habitat surveyed within the 30 –50 m depth range occupying 41% of the total area surveyed. The Spur and Groove habitat resembled a neritic habitat that extends until the bank's shallower margin. It is the habitat where spawning aggregations of red hind (Epinephelus guttatus) had been reported. The Path Reefs were mainly found near the boundaries of the Bank Coral Reef at the deep basin walls, occupying 9.3% of the total area surveyed. The Colonized Rhodolith Reef habitats were observed mainly down the insular slope of the outer shelf break, occupying 14.9 % of the monitored area. The Bank Coral Reef showed a relatively high composition of live coral cover. However, sponges are the most diverse group of benthic organisms in LB, with twice as many species as coral species.

Figure 23. Benthic habitat map of Lang Bank, St. Croix USVI (from García-Sais et al. 2014).

7.3 Condition and changes through time of marine ecosystems within LB TCRMP, run by UVI scientists, has a permanent sampling site at LB (17,82372 N and -64,44943 W). This sampling area is named "Lang Hind site" (Ennis et al., 2019). Lang Hind was initially monitored in 2001 at a site on the shallower (24 m) portion of the bank to the west. Monitoring in 2004-2007 occurred along random transects in a deeper part of the reef (~33 m depth), and benthic transects were made permanent in this site in 2009. According to Ennis et al. (2019), the main threat at the Lang Hind site is that the aggregation site is near the closure boundary. Changes in benthic community structure, coral health, and reef fish are summarized below.

7.3.1 Benthic community structure According to Ennis et al. (2019) Lang Hind has a diverse sessile epibenthic community dominated by hard corals, predominantly Orbicella spp., gorgonians, and sponges. Coral cover at this site was affected in less extent by the 2005 bleaching event. Since 2009 coral cover has remained relatively stable (fig. 24a). The algal community is dominated by epilithic algal communities, although Lobophora variegata and filamentous cyanobacteria are also important. The algal community shows high inter-annual variability (fig 24b).

7.3.2 Coral Health During this time of monitoring, the 2005 event has been the strongest event with a prevalence of 80% bleaching and an extent higher than 80%. The 2019 bleaching event had a prevalence of 40% and an extent less than 20% (figure 13) (Ennis et al., 2019).

Ennis et al. (2019) summarize the main changes in coral health at Lang Hind site during monitoring as follows: This site was heavily affected during the 2005 coral bleaching event, with a very high prevalence of corals that were 100% bleached over the colony surface. Non-thermal bleaching with moderate prevalence and low extent on colonies also occurred in later years (particularly in 2019). Figure 24c shows bleaching prevalence and bleaching extent. The site was also heavily affected by white disease after the 2005 coral bleaching event and has had high disease prevalence in all years of monitoring. Figure 24d shows disease prevalence. Partial mortality showed a sudden increase after the 2005 bleaching event and was variable in later years. Recent partial mortality is unusually high largely as the result of fish bites and predation by the corallivorous snail Coralliophila spp. Figure 24e shows old and recent mortality prevalence.

7.3.3 Reef fish Lang Bank supports a red hind spawning association active during December through February each year (Ennis et al., 2019). One Nassau grouper was observed on the bank in 2011, the first observation across all St. Croix monitoring sites. There is reportedly a historic Nassau grouper spawning site near the Lang Hind monitoring site, and with the bank now closed to trap fishing, there is the hope for the re-establishment of the species on St. Croix. In 2018 a yellowfin grouper was reported on Lang Bank FSA.

Also, the TCRMP has observed in St. Croix, after years of absence, the Nassau grouper and the yellowfin grouper (Ennis et al., 2019). These encouraging findings should be followed within the framework of the management measures recently implemented in this marine reserve ( i.e., the bank is now closed to trap

fishing). On the other hand, lionfish have been reported since 2011, but its abundance has not increased significantly within this reserve. This is another aspect to follow up on.

Figure 24. Lang Bank benthic cover and coral health through time (mean ± SE). a, Coral cover; b, Cover of other benthic community components; c, Prevalence and extent of bleaching; d, Prevalence of reported diseases; e, Prevalence of old and recent mortality (from Ennis et al. 2019).

7.4 Reported species within LB TCRMP has a sampling site within MCD (Lang Hind). Additionally, in 2014 a study characterized this Marine Managed Area and found new benthic biota and reef fishes (García- Sais et al. 2014). The results from these studies on the benthic species and reef fish are summarized below.

There are 98 species/taxonomic groups of benthic algae, sponge, scleractinian corals, hydrocorals, and octocoral species reported within MCD (Table 17). The most abundant groups are algal turfs and the macroalgae Lobophora variegata. Sponges are the most diverse taxonomic group, with 53 recorded species. Among scleractinian corals, the most common is Orbicella franksii.

Table 17. Most representative benthic species recorded by TCRMP and Garcia- Saez et al, 2014 at the LB. Species/Groups Type Species/Groups Type Agaricia agaricites Scleractinian Briareum sp. Octocoral Agaricia grahamae Scleractinian Erythropodium caribaeorum Octocoral Agaricia lamarcki Scleractinian Eunicea spp. Octocoral Colpophyllia natans Scleractinian Muriceopsis spp. Octocoral Diploria labyrinthiformis Scleractinian Plexaurella sp. Octocoral Dichocoenia stokesii Scleractinian Pseudoplexaura sp. Octocoral Eusmilia fastigiata Scleractinian Pterogorgia sp. Octocoral Helioseris cucullata Scleractinian Agelas clathrodes Sponge Madracis areolata Scleractinian Agelas conifera Sponge Madracis decactis Scleractinian Amphimedon compressa Sponge Meandrina meandrites Scleractinian Clionia delitrix Sponge Montastraea cavernosa Scleractinian Geodia neptuni Sponge Mycetophyllia ferox Scleractinian Ircinia campana Sponge Orbicella faveolata Scleractinian Niphates erecta Sponge Orbicella franksii Scleractinian Verongula sp. Sponge Porites astreoides Scleractinian Xestospongia muta Sponge Porites porites Scleractinian Dictyota sp. Macroalgae Pseudodiploria strigosa Scleractinian Halimeda sp. Macroalgae Siderastrea siderea Scleractinian Lobophora sp. Macroalgae Stephanocoenia intersepta Scleractinian Stypopodium sp. Macroalgae Millepora alcicornis Scleractinian Turf algae * Turf Antillogorgia sp. Octocoral Filamentous cyanobacteria ** Cyanobacteria The fish community at MCD is composed of 115 species (Tables 18 and 19). Table 18 shows the commercially important fish species with their fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005), conservation status according to the IUCN red list, and trophic group according to Ennis et al. (2019). The commercially important species registered at MCD are groupers (red hind, coney, graysby) and snappers (mutton snapper, mahogany snapper, schoolmaster). Table 19 shows representative fish species found at this site and their fisheries status

according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005). Note that since 2011, the presence of the lionfish was already registered in this Marine Managed Area.

Table 18. Representative commercially important fish species recorded by TCRMP and Garcia- Saez et al, 2014 at the LB.

Scientific Name1 Common Name1 Fisheries2 UICN Red List Status3 Trophic Group1 Graysby Groupers Least Concern Piscivore Cephalopholis cruentatafulva Coney Groupers Least Concern Invertivore Epinephelus guttatus Red hind Groupers Least Concern Invertivore Epinephelus striatus Nassau grouper Groupers Critically Endangered Piscivore Mycteroperca interstitialis Yellowmouth grouper Groupers Vulnerable Piscivore Mycteroperca tigris Tiger grouper Groupers Data Deficient Piscivore Mycteroperca venenosa Yellowfin grouper Groupers Near Threatened Piscivore Paranthias furcifer Creolefish Groupers Least Concern Planktivore Lutjanus analis Mutton snapper Snappers Near Threatened Piscivore Lutjanus apodus Schoolmaster Snappers Least Concern Piscivore Lutjanus buccanella Blackfin snapper Snappers Data Deficient Piscivore Lutjanus cyanopterus Cubera snapper Snappers Vulnerable Piscivore Lutjanus griseus Gray snapper Snappers Least Concern Piscivore Lutjanus jocu Dog snapper Snappers Data Deficient Piscivore Lutjanus mahogani Mahogany snapper Snappers Least Concern Piscivore Lutjanus synagris Lane snapper Snappers Near Threatened Piscivore Ocyurus chrysurus Yellowtail snapper Snappers Data Deficient Planktivore Caranx bartholomaei Yellow jack Jacks Least Concern Piscivore Caranx crysos Blue runner Jacks Least Concern Piscivore Caranx latus Horse eye jack Jacks Least Concern Piscivore Caranx lugubris Black jack Jacks Least Concern Piscivore Caranx ruber Bar jack Jacks Least Concern Piscivore Seriola rivoliana Almaco jack Jacks Least Concern Piscivore Balistes vetula Queen trigger Triggerfish Near Threatened Invertivore Canthidermis sufflamen Ocean trigger Triggerfish Least Concern Planktivore Holacanthus ciliaris Queen angel Angelfish Least Concern Invertivore Pomacanthus arcuatus Gray angel Angelfish Least Concern Spongivore Pomacanthus paru French angel Angelfish Least Concern Invertivore Scarus guacamaia Rainbow parrotfish Parrotfishes Near Threatened Herbivore Scarus taeniopterus Princess parrotfish Parrotfishes Least Concern Herbivore Scarus vetula Queen parrotfish Parrotfishes Least Concern Herbivore Sparisoma aurofrenatum Redband parrotfish Parrotfishes Least Concern Herbivore Sparisoma rubripinne Yellowtail parrotfish Parrotfishes Least Concern Herbivore Sparisoma viride Stoplight parrotfish Parrotfishes Least Concern Herbivore 1 From Ennis et al. 2019; 2 According to CFMC 2005; 3 According to UICN Red List Status

Table 19. Other fish species recorded by TCRMP and Garcia- Saez et al, 2014 at the LB. Scientific Name1 Common Name1 Fisheries2

Cantherhines macrocerus Whitespotted filefish Triggerfish Melichthys niger Black durgon Triggerfish Xanthichthys ringens Sargassum triggerfish Triggerfish Mulloidichthys martinicus Yellow goatfish Goatfish Pseudupeneus maculatus Spotted goatfish Goatfish Anisotremus virginicus Porkfish Grunt Haemulon aurolineatum Tomtate Grunt Haemulon flavolineatum French grunt Grunt Haemulon plumierii White grunt Grunt Haemulon sciurus Bluestriped grunt Grunt Holocentrus adscensionis Squirrelfish Squirrelfish Holocentrus rufus Longspine squirrelfish Squirrelfish Myripristis jacobus Blackbar soldierfish Squirrelfish Holocentrus rufus Longspine squirrelfish Squirrelfish Myripristis jacobus Blackbar soldierfish Squirrelfish Acanthurus bahianus Ocean surgeonfish Surgeonfish Acanthurus chirurgus Doctorfish Surgeonfish Acanthurus coeruleus Blue tang Surgeonfish Malacanthus plumieri Sand tilefish Tilefish Bodianus rufus Spanish hogfish Wrasses Lachnolaimus maximus Hogfish Wrasses Pterois volitans Lionfish - Scomberomorus regalis Cero - Sphyraena barracuda Great barracuda - Dasyatis americana Southern stingray - Carcharhinus perezi Caribbean reef shark - Ginglymostoma cirratum Nurse shark -

7.5 Primary scientific studies that have or are taking place within LB The primary fisheries scientific studies at LB are summarized below.

Nemeth et al. (2007) compared the spatial and temporal patterns of red hind (Epinephelus guttatus) movements and migrations from annual spawning aggregations on St. Thomas (MCD) and St. Croix (Lang Bank). Around St. Thomas, E. guttatus migrated 6–33 km from a functional spawning area of 500 km2, and around St. Croix, E. guttatus migrated 5–18 km from a place 90 km2 apart. Similar movement timing, temporal and spatial changes in sex ratios, annual and lunar predictability were synchronized with

environmental cues. E. guttatus spawning aggregations in the Virgin Islands occur between the winter solstice (i.e., after December 20) and February 20 of every year and show a distinctive peak 20–40 days after the winter solstice.

García-Sais et al. (2014) characterized the mesophotic habitats of LB. Also, they conducted an independent fishery survey of 22 commercially important fish and two shellfish species (queen conch and spiny lobster). Only the two shellfish and four fish species were represented by more than 15 individuals in this fishery- independent survey. The main findings of these surveys are presented below. The invasive lionfish (Pterois sp.), species with potential commercial value as food, was the most abundant fish larger than 25 cm and occurred within the entire mesophotic depth range studied. Red hind (Epinephelus guttatus) showed densities within the range estimated from visual surveys at other mesophotic habitats within the Caribbean basin. Mutton snapper (Lutjanus analis) was the most abundant commercially important snapper observed from all benthic habitats studied. The queen triggerfish (Balistes vetula) was observed from all mesophotic habitats. It showed sizes near the maximum length reported for the Caribbean, suggesting that their population at mesophotic habitats from LB are not severely overfished. Queen conch (Strombus gigas) were observed in very high densities (up 50 Ind/1000m2) but mainly concentrated on Colonized Rhodolith Reef habitats. Spiny lobsters (Panulirus argus) were highly abundant at LB, particularly at the Colonized Pavement habitat.

Kadison et al. (2017) used two long-term fisheries independent datasets, collected by the U.S. Virgin Islands Territorial Coral Reef Monitoring Program and the National Oceanographic and Atmospheric Administration Center for Coastal Monitoring and Assessment, to compare both the occurrence and size of several species of large and commercially important reef fishes between the northern USVI St. Thomas and St. John) and St. Croix. These fishes are primarily apex piscivores and generally the first species overexploited in small-scale fisheries. The disparities between the fish communities on the two island shelves cannot be explained solely by differences in habitat (coral cover, rugosity) or fisheries management, such as the relative amount of marine protected area in local waters. They are instead probably caused by a combination of several other interrelated factors, including water depth, fishing methodology, fishable area, and the presence or absence of viable fish spawning areas. The authors discuss the positive effects of the proximity of the two reserves (GB and MCD) and a wide island shelf. In contrast, LB and MSSA are more isolated and surrounded by a narrower island platform. The authors suggest that St. Croix is an example of a severely overfished Caribbean island. This study illustrates the need to manage artisanal fisheries that are tailored to the physical and spatial constraints imposed by shallow insular platforms.

8. Mutton Snapper Spawning Aggregation (MSSA)

8.1 History and description of MSSA The NMFS using the MSFC & M Act, established the Mutton Snapper Fish Spawning Aggregation area (MSSA) in 1993 as a part of a rule that intended to protect and conserve the highly exploited mutton snapper (Lutjanus analis) populations (Federal Register 1993). In 1996, NMFS added a technical change to the regulations to alter the boundary of the MSSA area to make it compatible with USVI regulations (Federal Register 1996). MSSA is located in the territorial waters of USVI offshore SW St. Croix is located at A 17°37.8' N 64°53.0' W; B 17°39.0' N 64°53.0' W; C 17°39.0' N 64°50.5' W; D 17°38.1' N 64°50.5' W; E 17°37.8' N 64°52.5' W (Fig. 25).. The total area is total area: 8.9 km2, and the no-take area is 8.9 km2. MSSA is governed by the Caribbean Fisheries Management Council (CFMC), The National Oceanographic and Atmospheric Agency (NOAA), and the Virgin Islands Department of Natural Resources (VI-DPNR). MSSA is a seasonal no-take zone with a closure initially from March 1 to June 30 and amended in 2005 to April 1 to June 30 (Pittman et al. 2014, Schärer-Umpierre et al., 2014).

Figure 25. Location of the Mutton Snapper Spawning Aggregation (MSSA) with the locations of the main studies done at MSSA.

8.2 Marine ecosystems present in MSSA MSSA is recognized as an offshore shallow reef (Ennis et al. 2019). MSA is located 4 km off the southwestern point of the island of St. Croix (USVI). Kojis and Quinn (2011) described the habitat types present within this Marine Management Area. They identified eight habitat types: coral limestone, gorgonian plains, dense algae, sparse algae, algae on sand, algae and invertebrates, sand invertebrates, sand no ripple, sand ripple (Figure 26). Coral limestone habitat corresponds with a spur and groove coral reef and is the habitat with the greatest structural complexity. Most of the other habitats are flat areas with a diverse cover of biota. The spur and groove reef´s sessile epibenthic animal community is dominated by the boulder star coral (Orbicella spp.), with sub-dominance of sponges.

Figure 26 . Benthic habitats presented at Mutton Snapper FSA (Kojis and Quinn 2011).

8.3 Condition and changes through time of marine ecosystems in MSSA The TCRMP, carried out by scientists of the UVI, has a permanent sampling site at MSA. This sampling point is named “Mutton Snapper FSA site”, 24 m depth, at 17,63660 N and -64,86240 W, and has been monitored since 2003. Ennis et al. (2019) showed the prevalence and extent of bleaching at TCRMP sites (figure 13). In the case of the Mutton Snapper FSA site the 2005 event was the strongest, with a prevalence close to 100% and an extent higher than 90%. The 2019 bleaching event had a prevalence higher than 50% and an extent close to 20%. According to Ennis et al. (2019) the main threats at Mutton Snapper site are: i) Fishing pressure as evidenced by the numerous fishing line and fishing trap debris. ii) Susceptibility to long-term seawater warming. The main documented changes are summarized below.

8.3.1 Benthic community structure According to Ennis et al. (2019) the Mutton Snapper site’s sessile epibenthic animal community is dominated by the boulder star coral (Orbicella spp.), with sub-dominance of sponges. This site lost an extreme amount of coral cover (87.0%) in the 2005 coral bleaching event and has not regained any cover as of 2011 (fig. 27a). Since 2011 coral cover has remained relatively stable but with very low values. The algal community is co-dominated by the macroalgae Lobophora variegata and epilithic algae. Since 2005 macroalgae and filamentous cyanobacteria cover has shown an apparent increase. Filamentous cyanobacteria reached extreme cover values (57.7%) in 2009 (fig. 27b). Current levels of herbivory no longer appear to be able to control algal abundance.

Figure 27. Mutton Snapper benthic cover and coral health through time (mean ± SE). a, Coral cover; b, Cover of other benthic community components; c, Prevalence and extent of bleaching; d, Prevalence of reported diseases; e, Prevalence of old and recent mortality (modified from Ennis et al. 2019).

8.3.2 Coral Health In the case of the Mutton Snapper FSA site the 2005 event was the strongest, with a prevalence close to 100% and an extent higher than 90%. The 2019 bleaching event had a prevalence higher than 50% and an extent close to 20% (Figure 27c). Bleaching prevalence has remained high for most years since 2005, but at low colony extent, indicating continued impairment of corals. There was an increase in the percentage of corals experiencing bleaching in 2019 at a predicted 6 DWH. White disease has been at consistently high values through many years of monitoring. Figure 27d shows disease prevalence. Partial mortality increased after 2005, and then whole colonies were lost from the system. Impairment of this site is puzzling as stressors besides fishing appear to be low. Clear water and low genetic diversity of corals may increase susceptibility to environmental stress and white disease. Figure 27e shows old and recent mortality prevalence (Ennis et al., 2019).

8.3.3 Reef fish The Mutton Snapper site is an offshore, shelf edge site with a diverse and rich fish community. Mutton Snapper site is reportedly in an area that mutton snapper spawn, however this species has been rare in surveys conducted at the site over the years. On the other hand, the lionfish have been observed regularly on Mutton Snapper, since his first sight in 2012, probably because the reef is offshore and does not receive the recreational diving and hunting pressure of nearshore sites (Ennis et al. 2019).

8.4 Reported species within MSSA TCRMP has a sampling site within MSSA (Lang Hind). Additionally, in 2011 a study characterized this Marine Managed Area and found new benthic biota and reef fishes (Kojis and Quinn 2011). The results from these studies on the benthic species and reef fish are summarized below.

There are 25 species/taxonomic groups of benthic algae, sponge, scleractinian corals, hydrocorals, and octocoral species reported within MSSA (Table 20). The most abundant groups are algal turfs and the macroalgae Lobophora variegata. Among scleractinian corals, the most common is Orbicella franksii.

The fish community at MSSA is composed of 134 species (Tables 21 and 22). Table 21 shows the commercially important fish species with their fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005), conservation status according to the IUCN red list, and trophic group according to Ennis et al. (2019). The commercially important species registered at MCD are groupers (red hind, coney, graysby) and snappers (mahogany snapper, yellowtail snapper). Table 22 shows representative fish species found at this site and their fisheries status according to the Caribbean Reef Fish FMU (Fisheries Management Unit) proposed by CFMC (2005). Note that since 2012, the presence of the lionfish was already registered in this Marine Managed Area.

Table 20. Most representative benthic species reported by TCRMP, Kojis and Quinn, 2011 at the MSSA. Species/Groups Type Species/Groups Type

Agaricia lamarcki Scleractinian Sea Fan Octocoral Agaricia sp. Scleractinian Clionia delitrix Sponge Eusmilia fastigiata Scleractinian Encrusting sponge Sponge Montastraea cavernosa Scleractinian Sponge Sponge Madracis decactis Scleractinian Macroalgae Macroalgae Orbicella faveolata Scleractinian Cladophora spp. Macroalgae Orbicella franksii Scleractinian Dictyota spp. Macroalgae Porites astreoides Scleractinian Lobophora variegata Macroalgae Porites porites Scleractinian Macroalgae Macroalgae Stephanocoenia intersepta Scleractinian Peyssonellia spp. Calcareous Macroalgae Siderastrea siderea Scleractinian Coralline algae Calcareous Millepora alcicornis Hydrocoral Turf algae Turf Erythropodium caribaeorum Octocoral Filamentous cyanobacteria Cyanobacteria

Table 21. Representative commercially important fish species reported by TCRMP at MSSA (from Kojis and Quinn, 2011). Scientific Name1 Common Name1 Fisheries2 UICN Red List Status3 Trophic Group1

Cephalopholis cruentata Graysby Groupers Least Concern Piscivore Cephalopholis fulva Coney Groupers Least Concern Invertivore Epinephelus adscensionis Rock hind Groupers Least Concern Invertivore Epinephelus guttatus Red hind Groupers Least Concern Invertivore Epinephelus striatus Nassau grouper Groupers Critically Endangered Piscivore Paranthias furcifer Creolefish Groupers Least Concern Planktivore Lutjanus analis Mutton snapper Snappers Near Threatened Piscivore Lutjanus apodus Schoolmaster Snappers Least Concern Piscivore Lutjanus cyanopterus Cubera snapper Snappers Vulnerable Piscivore Lutjanus griseus Gray snapper Snappers Least Concern Piscivore Lutjanus mahogani Mahogany snapper Snappers Least Concern Piscivore Lutjanus synagris Lane snapper Snappers Near Threatened Piscivore Ocyurus chrysurus Yellowtail snapper Snappers Data Deficient Planktivore Caranx bartholomaei Yellow jack Jacks Least Concern Piscivore Caranx crysos Blue runner Jacks Least Concern Piscivore Caranx lugubris Black jack Jacks Least Concern Piscivore Caranx ruber Bar jack Jacks Least Concern Piscivore Seriola rivoliana Almaco jack Jacks Least Concern Piscivore

Balistes vetula Queen trigger Triggerfish Near Threatened Invertivore Canthidermis sufflamen Ocean trigger Triggerfish Least Concern Planktivore Holacanthus ciliaris Queen angel Angelfish Least Concern Invertivore Pomacanthus arcuatus Gray angel Angelfish Least Concern Spongivore Pomacanthus paru French angel Angelfish Least Concern Invertivore Scarus coelruleus Blue parrotfish Parrotfishes Least Concern Herbivore Scarus taeniopterus Princess parrotfish Parrotfishes Least Concern Herbivore Scarus vetula Queen parrotfish Parrotfishes Least Concern Herbivore Sparisoma aurofrenatum Redband parrotfish Parrotfishes Least Concern Herbivore Sparisoma chrysopterum Redtail parrotfish Parrotfishes Least Concern Herbivore Sparisoma rubripinne Yellowtail parrotfish Parrotfishes Least Concern Herbivore Sparisoma viride Stoplight parrotfish Parrotfishes Least Concern Herbivore 1 From Ennis et al. 2019; 2 According to CFMC 2005; 3 According to UICN Red List Status

Table 22. Other fish species reported by TCRMP, Kojis and Quinn, 2011 at MSSA. Scientific Name1 Common Name1 Fisheries2

Caranx hippos Crevalle jack Jacks Cantherhines macrocerus Whitespotted filefish Triggerfish Melichthys niger Black durgon Triggerfish Xanthichthys ringens Sargassum triggerfish Triggerfish Mulloidichthys martinicus Yellow goatfish Goatfish Pseudupeneus maculatus Spotted goatfish Goatfish Anisotremus surinamensis Black margate Grunt Anisotremus virginicus Porkfish Grunt Haemulon aurolineatum Tomtate Grunt Haemulon flavolineatum French grunt Grunt Haemulon plumierii White grunt Grunt Haemulon sciurus Bluestriped grunt Grunt Holocentrus adscensionis Squirrelfish Squirrelfish Holocentrus rufus Longspine squirrelfish Squirrelfish Myripristis jacobus Blackbar soldierfish Squirrelfish Holocentrus rufus Longspine squirrelfish Squirrelfish Myripristis jacobus Blackbar soldierfish Squirrelfish Acanthurus bahianus Ocean surgeonfish Surgeonfish Acanthurus chirurgus Doctorfish Surgeonfish Acanthurus coeruleus Blue tang Surgeonfish Malacanthus plumieri Sand tilefish Tilefish Bodianus rufus Spanish hogfish Wrasses Lachnolaimus maximus Hogfish Wrasses

Pterois volitans Lionfish - Scomberomorus regalis Cero - Sphyraena barracuda Great barracuda - Dasyatis americana Southern stingray - Carcharhinus perezi Caribbean reef shark - Ginglymostoma cirratum Nurse shark - 1 From Ennis et al. 2019; 2 According to CFMC 2005.

8.5 Primary scientific studies that have or are taking place within MSSA

The primary fisheries scientific studies at MSSA are summarized below.

Kojis and Quinn (2011) described the benthic habitats of MSSA. Also, they conducted during 2009 and 2010 an study to provide information on the status of the Lutjanus analis spawning aggregation on the southwestern insular shelf of St. Croix, USVI, verify the spawning period for this species, and provide life history information. The authors attempted to observe the reproductive aggregation of this snapper at the historically recognized time and site, but did not observe such an event. Faced with this scenario, they conducted a CPU study that showed very important information. Based on this CPUE survey the authors concluded that the spawning aggregation of mutton snapper in or near the MSSA appears to be fairly robust. This is despite fairly heavy fishing pressure that continued until the seasonal prohibition on possession of mutton snapper in territorial and federal waters 2006 went into effect. The skewed sex ratio of the catches, a result of a high proportion of small males, which start reproducing at a smaller size than females, may reflect high fishing pressure before 2006 and the initial recovery of the population. Given the high female fecundity reported in this study, recovery may occur quickly if fishers continue to respect the seasonal possession prohibition and enforcement is adequate.The authors suggested that the actual site of the mutton snapper aggregation still needs to be confirmed, and proposed a new site that will be checked to identify the currently spawning site.

9. General discussion, gaps and recommendations

Coral reef habitats should provide essential habitat (i.e., spawning grounds) for the survival of commercially important species. This premise, while intuitive, should be based on scientific studies in these MMAs. From our review of the information, we could not find studies that explicitly test if coral reef habitats are necessary beyond spawning aggregations (i.e., feeding grounds) for commercially important species and what role they play in the recovery of their populations. If coral reefs are essential for the sustainability of fish populations, then a continuous monitoring program of these reef areas is imperative. Monitoring efforts should be based on permanent transects that would allow estimating changes through time and the current state of the benthic communities. Currently, only a few of the MMAs (i.e., Grammanik Bank) have this monitoring in place. All others have only been characterized once (i.e., Bajo de Sico) or surveyed in different years at different habitats or depths, making comparisons inadequate across time.

The MMAs summarized in this report were created to manage and allow the recovery of different commercially important fish species. Management measures in locations such as the Grammanik Bank and the Marine Conservation District seem to be working and have allowed the recovery of some fish populations. We recommend periodic (every five years) stock assessment analysis of the top commercially important species to understand the current status of their populations. Such an analysis would serve as the baseline for future comparisons that would allow us to determine if populations are declining and adjust management efforts accordingly.

Acoustic tagging and telemetry could also be implemented more broadly across the MMAs to complement fisheries-based assessments. These telemetry approaches provide 1) Identifying specific habitats within MMAs that fishes use for reproduction or feeding. 2) Provide a powerful tool to evaluate the effectiveness of management strategies, the optimal MMA size, ecological connectivity (adult movement) among MMAs, and selection of nearby protected areas. 3) Provide baseline information about multispecies spawning aggregations. 5) Long-term acoustic monitoring can determine if spawning aggregation shifts spatially or temporally and the extent of the spawning season within MMAs, allowing managers to adjust conservation measures (i.e., extend closure times).

New technologies are becoming more available, easy to operate, and affordable. For instance, managers can use drones to quantify the presence and quantity of fishers during banning times and design patrolling activities based on these observations. Similarly, underwater drone-type equipment coupled with high- resolution cameras guided by virtual reality and GIS adjusted maps could provide a new way to give a more comprehensive way to monitor benthic and fish communities. Videos also have the added value that can be reanalyzed in the future if needed.

From our literature review, most MMAs and MPAs have been established as individual sites of local significance rather than synergistic interconnected components of a broader network. Evidence, however, indicates that ecological connectivity enhances the effectiveness, biodiversity, productivity, stability, and resilience of marine protected areas (MPAs) and MMAs. For example, the structure of marine communities and the performance of an MMA/MPA in replenishing fish populations can be influenced by connectivity among coastal marine ecosystems and offshore habitat, with well-documented examples including interconnected nursery habitats, ontogenetic shifts to deeper water, migrations to spawning aggregations,

and larval supply. The need for improved information on ecological connectivity within the US Caribbean is evident and urgent. Targeted transdisciplinary scientific research and decision support tools that explicitly incorporate ecological connectivity into the design and management of MMA and MPA networks are required to support near-term capacity building for managers across the US Caribbean.

The US Caribbean hosts a collection of protected areas linking land and sea, some with high biodiversity, cultural importance, and increasing vulnerability to human activities, including climate change. There are 58 areas with some level of protection, including areas managed by the CFMC and areas managed by the PR or USVI Departments of Natural Resources. From our review, it is clear that most areas are managed as single units and not as networks of protected areas. We thus recommend the different managing agencies generating a committee/task force that begins the coordination of activities across the various protected areas and design strategies that incorporate the network nature of these managed areas. This committee should also coordinate monitoring programs and scientific efforts to understand the level of connectivity across the different protected areas and the habitats within and among the various protected areas.

In our revision of the scientific literature, we only found two studies (Jackson et al., 2014; Bernard et al., 2016) addressing whether larvae from populations in Grammanik Bank are self-sustained. Authors of both studies suggest that larvae are instead coming from areas outside the US Virgin Island with high connectivity across populations. However, models of passive particles indicate that populations in the USVI are self-maintained with a high probability of local recruitment (Canals 2019). These ambiguous findings warrant further evaluation of the nature of recruitment in these areas. A comprehensive study of genetic analysis should address whether the 58 protected areas in the US Caribbean are self-sustained, or if instead, they depend on larvae/recruits coming from the lesser Antilles, the Bahamas, or the Dominican Republic. It should also incorporate a Caribbean-wide connectivity analysis of the top commercial species (and the main coral species that provide habitat to those fish populations) to understand if populations in the US Caribbean are different stocks from those in Florida, the Bahamas, and the Mesoamerican reefs.

Some observations point out to spawning behaviors of previously unreported species. For example, Garcia et al., 2013 observed at Tourmaline Bank the reproductive behavior of two species, Lutjanus jocus and Lutjanus cyanopterus. We recommend new studies using acoustic tagging to understand these species' spawning behavior further and test whether the MMA is also allowing the recovery of populations in these two species.

All collected data (i.e., SEMAP) from and all locations should be made publicly available and easy to download so that managers and researchers can use it to analyze patterns either on the benthic community or fish populations. Publicly available data facilitates work by managing agencies, decreases chances for duplicating efforts, stimulates research, and allows for analysis of changes through time of the habitats within these MMAs.

10. References

Appeldoorn, R., Alfaro, M., Ballantine, D., Bejarano, I., Ruiz, H., Schizas, N., et al. (2019). Puerto Rico. pp. 111– 129. Appeldoorn, R.S., Schärer-Umpierre, M.T., Rowell, T.J. & Nemeth, M. (n.d.). Usando la Producción del Sonido como Medida de las Densidades Relativas del Mero Cabrilla (Epinephelus guttatus) durante la Agregación de Desove: Consistencia Dentro y entre Los Lugares, 3. Appledoorn, E., Zayas, C., Sharer, M., Clouse, K. & Appledoorn, R. (2018). Temporal Patterns Among Multiple Courtship Associated Sounds in the Red Hind Epinephelus guttatus Indicate Two Spawning Aggregations During a Single Lunar Cycle. Proceedings of the 71st Gulf and Caribbean Fisheries Institute, GCFI 71. Armstrong, R.A., Singh, H., Torres, J., Nemeth, R.S., Can, A., Roman, C., et al. (2006). Characterizing the deep insular shelf coral reef habitat of the Hind Bank marine conservation district (US Virgin Islands) using the Seabed autonomous underwater vehicle. Continental Shelf Research, 26, 194–205. Baker, N., Appeldoorn, R. & Torres-Saavedra, P. (2016). Fishery-Independent Surveys of the Queen Conch Stock in Western Puerto Rico, with an Assessment of Historical Trends and Management Effectiveness. Marine and Coastal Fisheries Dynamics Management and Ecosystem Science, 8, 567–579. Baker, N., Appledoorn, R. & Torres-Saavadra, P.A. (2015). Population Trends and Management Effectiveness of Queen Conch, Strombus gigas, in Western Puerto Rico. Proceedings of the 68th Gulf and Caribbean Fisheries Institute, GCFI 68. Becker, S.L., Finn, J.T., Novak, A.J., Danylchuk, A.J., Pollock, C.G., Hillis-Starr, Z., et al. (2020). Coarse- and fine-scale acoustic telemetry elucidates movement patterns and temporal variability in individual territories for a key coastal mesopredator. Environ Biol Fish, 103, 13–29. Bernard, A., Feldheim, K., Richards, V., Nemeth, R. & Shivji, M. (2012). Development and characterization of fifteen novel microsatellite loci for the Nassau grouper (Epinephelus striatus) and their utility for cross- amplification on a suite of closely related species. Conservation Genetics Resources, 4, 983–986. Bernard, A.M., Feldheim, K.A., Nemeth, R., Kadison, E., Blondeau, J., Semmens, B.X., et al. (2016). The ups and downs of coral reef fishes: the genetic characteristics of a formerly severely overfished but currently recovering Nassau grouper fish spawning aggregation. Coral Reefs, 35, 11. Biggs, C. & Nemeth, R. (2016). Spatial and temporal movement patterns of two snapper species at a multi-species spawning aggregation. Marine Ecology Progress Series, 558. Brandtneris, V.W., Brandt, M.E., Glynn, P.W., Gyory, J. & Smith, T.B. (2016). Seasonal Variability in Calorimetric Energy Content of Two Caribbean Mesophotic Corals. PLOS ONE, 11, e0151953. Bryan, D., Feeley, M., Nemeth, R., Pollock, C. & Ault, J. (2019). Home range and spawning migration patterns of queen triggerfish Balistes vetula in St. Croix, US Virgin Islands. Marine Ecology Progress Series, 616, 123– 139. Caribbean Fishery Management Council. (1985). Amendment 2 to the Fishery Management Plan for the Shallow- Water Reef Fish Fishery of Puerto Rico and the U.S. Virgin Islands. NOAA. Available at: https://repository.library.noaa.gov/view/noaa/18386. Last accessed 13 April 2021. Caribbean Fishery Management Council. (2005). Comprehensive Amendment to the Fishery Management Plans (FMPs) of the U.S. Caribbean to Address Required Provisions of the Magnuson-Stevens Fishery Conservation and Management Act. NOAA. Available at: https://repository.library.noaa.gov/view/noaa/18269. Last accessed 13 April 2021. Cherubin, L.M., Dalgleish, F., Ibrahim, A., Scharer-Umpierre, M., Nemeth, R. & Appledoorn, R. (2018). New Insights on Fish Spawning Aggregation Dynamics from Autonomous Robotic Platform. GCFI 71. Chérubin, L.M., Dalgleish, F., Ibrahim, A.K., Schärer-Umpierre, M., Nemeth, R.S., Matthews, A., et al. (2020). Fish Spawning Aggregations Dynamics as Inferred From a Novel, Persistent Presence Robotic Approach. Front. Mar. Sci., 6.

Cherubin, L.M., Nemeth, R.S. & Idrisi, N. (2011). Flow and transport characteristics at an Epinephelus guttatus (red hind grouper) spawning aggregation site in St. Thomas (US Virgin Islands). Ecological Modelling, 222, 3132–3148. Day, J., Dudley, N., Hockings, M., Holmes, G., Laffoley, D., Stolton, S., et al. (2019). Guidelines for applying the IUCN protected area management categories to marine protected areas. ( No. Second edition). IUCN, Gland. Switzerland. De’ath, G., Fabricius, K.E., Sweatman, H. & Puotinen, M. (2012). The 27–year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci USA, 109, 17995. Debrot, A., Brunel, T., Schop, J., Kuramae, A. & Bakkers, Y. (2020). Assessing effectiveness of the seasonal closure of the Moonfish Bank of the Saba Bank for two species of concern, the Red Hind and the Queen Triggerfish: the first five years. Ennis, R., Kadison, E., Heidmann, S., Brandt, M., Henderson, L. & Smith, T. (2019). The United States Virgin Islands TERRITORIAL CORAL REEF MONITORING PROGRAM Annual Report (Annual Report). TERRITORIAL CORAL REEF MONITORING PROGRAM. The Center for Marine and Environmental Studies, University of the Virgin Islands, The Division of Coastal Zone Management, USVI Department of Planning and Natural Resources, The Coral Reef Conservation Program, National Oceanic and Atmospheric Administration. Federal Register Vol. 54, No.235, December 8, 1989 - Content Details - FR-1989-12-08. (2021). Federal Register. Available at: https%3A%2F%2Fwww.govinfo.gov%2Fapp%2Fdetails%2FFR-1989-12-08. Last accessed 13 April 2021. Federal Register Vol. 55, No.135, July 13, 1990 - Content Details - FR-1990-07-13. (2021). Federal Register. Available at: https%3A%2F%2Fwww.govinfo.gov%2Fapp%2Fdetails%2FFR-1990-07-13. Last accessed 13 April 2021. Federal Register Vol. 55, No.213, November 2, 1990 - Content Details - FR-1990-11-02. (2021). Federal Register. Available at: https%3A%2F%2Fwww.govinfo.gov%2Fapp%2Fdetails%2FFR-1990-11-02. Last accessed 13 April 2021. Federal Register Vol. 58, No.139, July 22, 1993 - Content Details - FR-1993-07-22. (2021). Federal Register. Available at: https%3A%2F%2Fwww.govinfo.gov%2Fapp%2Fdetails%2FFR-1993-07-22. Last accessed 13 April 2021. Federal Register Vol. 58, No.197, October 14, 1993 - Content Details - FR-1993-10-14. (2021a). Federal Register. Available at: https%3A%2F%2Fwww.govinfo.gov%2Fapp%2Fdetails%2FFR-1993-10-14. Last accessed 13 April 2021. Federal Register Vol. 58, No.197, October 14, 1993 - Content Details - FR-1993-10-14. (2021b). Federal Register. Available at: https%3A%2F%2Fwww.govinfo.gov%2Fapp%2Fdetails%2FFR-1993-10-14. Last accessed 13 April 2021. Federal Register Vol. 69, No.220, November 16, 2004 - Document in Context - FR-2004-11-16. (2021). Federal Register. Available at: https%3A%2F%2Fwww.govinfo.gov%2Fapp%2Fdetails%2FFR-2004-11- 16%2Fcontext. Last accessed 13 April 2021. García-Sais, J., Castro, R., Sabater-Clavell, J., Carlo, M., Esteves-Amador, R.F., Bruckner, A.W., et al. (2007). Characterization of benthic habitats and associated reef communities at Bajo de Sico seamount, Mona Passage, Puerto Rico final report. undefined. García-Sais, J., Castro-Gomez, R., Sabater-Clavell, J., Esteves, R., Williams, S. & Carlo, M. (2010). Mesophotic benthic habitats and associated marine communities at Abrir La Sierra, Puerto Rico. García-Sais, J., Williams, S., Esteves, R., Sabater, J. & Carlo, M. (2013). Characterization of mesophotic benthic habitats and associated reef communities at Tourmaline Reef, Puerto Rico. García-Sais, J., Williams, S., Esteves, R., Sabater, J. & Carlo, M. (2017a). MONITORING OF CORAL REEF COMMUNITIES FROM NATURAL RESERVES IN PUERTO RICO: 2017. García-Sais, J., Williams, S., Sabater, J. & Carlo, M. (2019). Puerto Rico Coral Reef Monitoring Program: 2019 Survey.

García-Sais, J., Williams, S., Sabater-Clavell, J., Esteves, R. & Carlo, M. (2014). Mesophotic benthic habitats and associated reef communities at Lang Bank, St. Croix, USVI. García-Sais, J.R., Sabater-Clavell, J., Esteves, R., Carlo, M. & Box, P.O. (n.d.). Fishery independent survey of commercially exploited fish and shellfish populations from mesophotic reefs within the Puertorrican EEZ, 91. García-Sais, J.R., Williams, S.M. & Amirrezvani, A. (2017b). Mortality, recovery, and community shifts of scleractinian corals in Puerto Rico one decade after the 2005 regional bleaching event. PeerJ, 5, e3611. Garcia-Sais, J.R., Williams, S.M., Sabater-Clavell, J. & Carlo, M. (2017). PROGRAMMATIC ACTIVITY 6- CORAL REEF MONITORING PROGRAM, 272. Gardner, T.A. (2003). Long-Term Region-Wide Declines in Caribbean Corals. Science, 301, 958–960. Groves, S., Holstein, D., Enochs, I., Kolodziej, G., Manzello, D., Brandt, M., et al. (2018). Growth rates of Porites astreoides and Orbicella franksi in mesophotic habitats surrounding St. Thomas, US Virgin Islands. Coral Reefs, 37. Holstein, D., Smith, T. & Gyory, J. (2015). Fertile fathoms: Deep reproductive refugia for threatened shallow corals. Scientific Reports, 5. Holstein, D.M., Smith, T.B. & Paris, C.B. (2016). Depth-Independent Reproduction in the Reef Coral Porites astreoides from Shallow to Mesophotic Zones. PLOS ONE, 11, e0146068. Ibrahim, A., Cherubin, L., Schärer, M., Zhuang, H. & Erdol, N. (2018a). Automatic classification of grouper species by their sounds using deep neural networks. The Journal of the Acoustical Society of America, 144. Ibrahim, A., Cherubin, L., Zhuang, H., Schärer, M., Dalgleish, F., Erdol, N., et al. (2018b). An approach for automatic classification of grouper vocalizations with passive acoustic monitoring. The Journal of the Acoustical Society of America, 143, 666–676. Ibrahim, A., Zhuang, H., Cherubin, L., Schärer, M., Muhamed Ali, A., Nemeth, R., et al. (2019). Classification of red hind grouper call types using random ensemble of stacked autoencoders. The Journal of the Acoustical Society of America, 146. Ibrahim, A., Zhuang, H., Cherubin, L., Schärer, M., Nemeth, R., Erdol, N., et al. (2020). Transfer learning for efficient classification of grouper sound. The Journal of the Acoustical Society of America, 148. Jackson, A.M., Semmens, B.X., Mitcheson, Y.S. de, Nemeth, R.S., Heppell, S.A., Bush, P.G., et al. (2014a). Population Structure and Phylogeography in Nassau Grouper (Epinephelus striatus), a Mass-Aggregating Marine Fish. PLOS ONE, 9, e97508. Jackson, J., Donovan, M. & Cramer, K. (2014b). Status and Trends of Caribbean Coral Reefs: 1970-2012 (Lam VV (editors)). Global Coral Reef Monitoring Network. IUCN, Gland, Switzerland. Jackson, J., Donovan, M., Cramer, K. & Lam, V. (2014c). Status and Trends of Caribbean Coral Reefs: 1970-2012. Jossart, J., Nemeth, R., Avram, P. & Stolz, R. (2017). Extreme passive acoustic telemetry detection variability on a mesophotic coral reef, United States Virgin Islands. Marine Biology, 164. Kadison, E. (2009). Nassau Grouper (Epinephelus striatus) in St. Thomas, US Virgin Islands, with Evidence for a Spawning Aggregation Site Recovery. Proceedings of the Sixty second Gulf and Caribbean Fisheries Society, 62, 273–279. Kadison, E., Brandt, M., Nemeth, R., Martens, J., Blondeau, J. & Smith, T. (2017). Abundance of commercially important reef fish indicates different levels of over-exploitation across shelves of the U.S. Virgin Islands. PLOS ONE, 12, e0180063. Kadison, E., Nemeth, R., Brown-Peterson, N., Blondeau, J., Smith, T. & Calnan, J. (2010). Yellowfin Grouper (Mycteroperca venenosa): Reproductive Biology, Behavior and Conservation of a Large Caribbean grouper. 63Proceedings of the Sixty Three Annual Gulf and Caribbean Fisheries Institute, 63, 157–160. Kadison, E., Nemeth, R., Herzlieb, S. & Blondeau, J. (2006). Temporal and spatial dynamics of Lutjanus cyanopterus (Pisces: Lutjanidae) and L. jocu spawning aggregations in the United States Virgin Islands. Rev. Biol. Trop., 54.

Kobara, S., Heyman, W., Pittman, S. & Nemeth, R. (2013). Biogeography of transient reef-fish spawning aggregations in the Caribbean: a synthesis for future research and management. Oceanography and marine biology, 51, 281–326. Kojis, B. & Quinn, N. (2010). INVESTIGATION OF THE SPAWNING AGGREGATION OF MUTTON SNAPPER, Lutjanus analis (Cuvier), ON THE SOUTHWESTERN SHELF OF ST. CROIX, U.S. VIRGIN ISLANDS. Kojis, B. & Quinn, N. (2011a). Distribution and Abundance of Fish Populations in Various Habitats in the Mutton Snapper (Lutjanus analis) Conservation Area on the South Shelf St. Croix, U.S. Virgin Islands. Kojis, B.L. & Quinn, N.J. (2011b). Validation of a Spawning Aggregation of Mutton Snapper and Characterization of the Benthic Habitats and Fish in the Mutton Snapper Seasonal Closed Area, St. Croix, US Virgin Islands. NOAA Coral Reef Grand Program, Caribbean Fishery Management Council San Juan, Puerto Rico. Kojis, B.L., Quinn, N.J. & Agar, J.J. (2017). Census of licensed fishers of the U.S. Virgin Islands (2016). Maher, R.L., Johnston, M.A., Brandt, M.E., Smith, T.B. & Correa, A.M.S. (2018). Depth and coral cover drive the distribution of a coral macroborer across two reef systems. PLOS ONE, 13, e0199462. Mann, D., Locascio, J., Schärer, M., Nemeth, M. & Appeldoorn, R. (2010). Sound production by red hind Epinephelus guttatus in spatially segregated spawning aggregations. Aquatic Biology - AQUAT BIOL, 10, 149–154. Marine Managed Areas and Fisheries, Volume 69 - 1st Edition. (2021). . Available at: https://www.elsevier.com/books/marine-managed-areas-and-fisheries/johnson/978-0-12-800214-8. Last accessed 13 April 2021. Marshak, A. & Appeldoorn, R. (2008). Evaluation of Seasonal Closures of Red Hind, Epinephelus guttatus, Spawning Aggregations to Fishing off the West Coast of Puerto Rico Using Fishery-dependent and Independent Time Series Data, 60, 566–572. Mitcheson, Y.S. de & Colin, P.L. (Eds.). (2012). Reef Fish Spawning Aggregations: Biology, Research and Management. Fish & Fisheries Series. Springer Netherlands. Mora, C. (2008). A clear human footprint in the coral reefs of the Caribbean. Proc. R. Soc. B., 275, 767–773. Nemeth, R. (2010). Dynamics of Reef Fish and Decapod Crustacean Spawning Aggregations: Underlying Mechanisms, Habitat Linkages, and Trophic Interactions. In: Ecological Connectivity among Tropical Coastal Ecosystems. pp. 73–134. Nemeth, R., Herzlieb, S. & Blondeau, J. (2006a). Comparison of two seasonal closures for protecting red hind spawning aggregations in the US Virgin Islands. Nemeth, R. & Kadison, E. (2013). Temporal patterns and behavioral characteristics of aggregation formation and spawning in the Bermuda chub (Kyphosus sectatrix). Coral Reefs, 32. Nemeth, R., Kadison, E., Blondeau, J., Idrisi, N., Watlington, R., Brown, K., et al. (2008). Regional coupling of red hind spawning aggregations to oceanographic processes in the eastern Caribbean. Nemeth, R., Kadison, E., Brown-Peterson, N. & Blondeau, J. (2019). Reproductive biology and behavior associated with a spawning aggregation of the yellowfin grouper Mycteroperca venenosa in the U.S. Virgin Islands. Bulletin of Marine Science, 96. Nemeth, R., Kadison, E., Herzlieb, S., Blondeau, J. & Whiteman, E. (2006b). Status of a Yellowfin (Mycteroperca venenosa) Grouper Spawning Aggregation in the US Virgin Islands with Notes on Other Species. Presented at the Proceedings of the Gulf and Caribbean Fisheries Institute. Nemeth, R. & Quandt, A. (2005). Differences in fish assemblage structure following the establishment of the Marine Conservation District, St. Thomas U. S. Virgin Islands. Nemeth, R.S. (2005). Population characteristics of a recovering US Virgin Islands red hind spawning aggregation following protection. Mar Ecol Prog Ser, 286, 81–97. Nemeth, R.S. (2021). Comparative Investigations of Red Hind (Epinephelus guttatus) spawning aggregations under different management strategies | Dutch Caribbean Biodiversity Database. Available at: https://www.dcbd.nl/document/comparative-investigations-red-hind-epinephelus-guttatus-spawning- aggregations-under. Last accessed 13 April 2021.

Nemeth, R.S., Blondeau, J., Herzlieb, S. & Kadison, E. (2007). Spatial and temporal patterns of movement and migration at spawning aggregations of red hind, Epinephelus guttatus, in the U.S. Virgin Islands. Environ Biol Fish, 78, 365–381. Nemeth, R.S., Blondeau, J. & Kadison, E. (2009). Defining marine protected areas for yellowfin and Nassau grouper spawning aggregation sites. Presented at the Proceedings of the Gulf and Caribbean Fisheries Institute, 61, pp. 329–330. Nemeth, R.S., Smith, T.B., Blondeau, J., Kadison, E., Calnan, J.M. & Gass, J. (2021). Characterization of deep water reef communities within the marine conservation district, St. Thomas, U.S. Virgin Islands final report. NOAA. Available at: https://repository.library.noaa.gov/view/noaa/568. Last accessed 13 April 2021. Novak, A., Becker, S., Finn, J.T. & Pollock, C.G. (n.d.). (PDF) Scale of Biotelemetry Data Influences Ecological Interpretations of Space and Habitat Use in Yellowtail Snapper. ResearchGate. Novak, A.J., Becker, S.L., Finn, J.T., Danylchuk, A.J., Pollock, C.G., Hillis-Starr, Z., et al. (2020). Inferring residency and movement patterns of horse-eye jack Caranx latus in relation to a Caribbean marine protected area acoustic telemetry array. Animal Biotelemetry, 8, 12. Ojeda-Serrano, E., Appledoorn, R. & Ruiz-Valentin, I. (2007a). “Reef fish Spawning Aggregations of the Puerto Rican Shelf” (Final Report). “Reef fish Spawning Aggregations of the Puerto Rican Shelf.” Caribbean Coral Reef Institute, Mayagüez, PR 00681-9013. Ojeda-Serrano, E., Appledoorn, R.S. & Ruiz-Valentine, I. (2007b). Reef Fish Spawning Aggregations of the Puerto Rican Shelf. 59th Gulf and Caribbean Fisheries Institute, GCFI 59. Pickard, A., Vaudo, J., Wetherbee, B., Nemeth, R., Blondeau, J. & Kadison, E. (2016). Comparative. Pittman, S.J., Bauer, L., Hile, S.D., Jeffery, C.F.G., Davenport, E. & Caldow, C. (2014a). Marine Protected Areas of the US Virgin Islands (Ecological Performance Report). NOS NCCOS 187. NOAA National Centers for Coastal Ocean Science, Silver Spring, MD 20910. Pittman, S.J., Monaco, M.E., Friedlander, A.M., Legare, B., Nemeth, R.S., Kendall, M.S., et al. (2014b). Fish with Chips: Tracking Reef Fish Movements to Evaluate Size and Connectivity of Caribbean Marine Protected Areas. PLOS ONE, 9, e96028. Quinn, N. (2010). Validation of a Mutton Snapper (Lutjanus analis) Spawning Aggregation in the Mutton Snapper Seasonal Closed Area, St. Croix, U.S. Virgin Islands. Quinn, N. & Kojis, B. (2011). Habitat Description of the St. Croix, U.S. Virgin Islands South Coast Mutton Snapper (Lutjanus analis) Seasonal Closed Area. Roberts, C.M. & Polunin, N.V.C. (1991). Are marine reserves effective in management of reef fisheries? Rev Fish Biol Fisheries, 1, 65–91. Robinson, W.L. (2009). Regulatory amendment to the fishery management plan for the reef fish fishery of Puerto Rico and the U.S. Virgin Islands modifying the Bajo de Sico seasonal closure including a regulatory impact review and an environmental assessment. NOAA. Available at: https://repository.library.noaa.gov/view/noaa/626. Last accessed 13 April 2021. Rodriguez-Ferrer, G., Cruz-Motta, J.J., Schizas, N.V. & Appeldoorn, R.S. (2020). Modelling distribution of the common bottlenose dolphin, Tursiops truncatus off the southwest coast of Puerto Rico. Journal of Marine Systems, 210, 103371. Rowell, T., Nemeth, R., Schärer, M. & Appeldoorn, R. (2015). Fish sound production and acoustic telemetry reveal behaviors and spatial patterns associated with spawning aggregations of two Caribbean groupers. Marine Ecology Progress Series, 518, 239–254. Rowell, T., Schärer, M. & Appeldoorn, R. (2018). Description of a New Sound Produced by Nassau Grouper at Spawning Aggregation Sites. Gulf and Caribbean Research, 29, 22–26. Rowell, T., Schärer, M., Appeldoorn, R., Nemeth, M., Mann, D. & Rivera, J. (2012). Sound production as an indicator of red hind density at a spawning aggregation. Marine Ecology Progress Series, 462, 241–250. Rowell, T.J., Appledoorn, R.S., Rivera, J.A., Mann, D.A., Kellison, T., Nemeth, M., et al. (2010). Use of Passive Acoustics to Map Grouper Spawning Aggregations, with Emphasis on Red Hind, Epinephelus guttatus, Off Western Puerto Rico. Proceedings of the 63rd Gulf and Caribbean Fisheries Institute, Use of Passive

Acoustics to Map Grouper Spawning Aggregations, with Emphasis on Red Hind, Epinephelus guttatus, Off Western Puerto Rico, GCFI 63. Sale, P., Cowen, R., Danilowicz, B., Jones, G., Kritzer, J., Lindeman, K., et al. (2005). Critical science gaps impede use of no-take fishery reserves. Trends in Ecology & Evolution, 20, 74–80. Sanders, I.M., Barrios-Santiago, J.C. & Appeldoorn, R. (2005). Distribution and relative abundance of humpback whales off western Puerto Rico during 1995-1997. Caribbean Journal of Science, 41, 101–107. Schärer, M., Nemeth, M., Mann, D., Locascio, J., Appeldoorn, R. & Rowell, T. (2012a). Sound Production and Reproductive Behavior of Yellowfin Grouper, Mycteroperca venenosa (Serranidae) at a Spawning Aggregation. Copeia, 1, 134–144. Schärer, M., Rowell, T., Nemeth, M. & Appeldoorn, R. (2012b). Sound production associated with reproductive behavior of Nassau grouper Epinephelus striatus at spawning aggregations. Endang. Species. Res., 19, 29– 38. Schärer, M., Zayas Santiago, C., Appeldoorn, R., Tuohy, E., Olson, J. & Keller, J. (2019). The Purr of the Lionfish: Sound and Behavioral Context of Wild Lionfish in the Greater Caribbean. Gulf and Caribbean Research, 30. Schärer, M.T., Nemeth, M.I., Rowell, T.J. & Appeldoorn, R.S. (2014). Sounds associated with the reproductive behavior of the black grouper (Mycteroperca bonaci). Mar Biol, 161, 141–147. Scharer-Umpierre, M., Pena-Al Verado, N., Smith, S.G., Appledoorn, R. & Ault, J.S. (2018). Deeper Water Fauna Caught Incidentally in the Puerto Rico Fishery. Proceedings of the 71st Gulf and Caribbean Fisheries Institute, GCFI 71. Smith, T., Ennis, R., Kadison, E., Nemeth, R. & Henderson, L. (2016a). The United States Virgin Islands TERRITORIAL CORAL REEF MONITORING PROGRAM Annual Report (Annual Report). TERRITORIAL CORAL REEF MONITORING PROGRAM. The Center for Marine and Environmental Studies, University of the Virgin Islands, The Division of Coastal Zone Management, USVI Department of Planning and Natural Resources, The Coral Reef Conservation Program, National Oceanic and Atmospheric Administration. Smith, T., Kadison, E., Henderson, L., Gyory, J., Brandt, M., Calnan, J., et al. (2011). The United States Virgin Islands TERRITORIAL CORAL REEF MONITORING PROGRAM Annual Report (Annual Report). TERRITORIAL CORAL REEF MONITORING PROGRAM. The Center for Marine and Environmental Studies, University of the Virgin Islands, The Division of Coastal Zone Management, USVI Department of Planning and Natural Resources, The Coral Reef Conservation Program, National Oceanic and Atmospheric Administration. Smith, T., Nemeth, R., Blondeau, J., Calnan, J.M., Kadison, E. & Herzlieb, S. (2008). Assessing coral reef health across onshore to offshore stress gradients in the US Virgin Islands. Marine Pollution Bulletin, 56, 1983– 1991. Smith, T.B., Blondeau, J., Nemeth, R.S., Pittman, S.J., Calnan, J.M., Kadison, E., et al. (2010). Benthic structure and cryptic mortality in a Caribbean mesophotic coral reef bank system, the Hind Bank Marine Conservation District, U.S. Virgin Islands. Coral Reefs, 29, 289–308. Smith, T.B., Brandt, M.E., Calnan, J.M., Nemeth, R.S., Blondeau, J., Kadison, E., et al. (2013). Convergent mortality responses of Caribbean coral species to seawater warming. Ecosphere, 4, art87. Smith, T.B., Brandtneris, V.W., Canals, M., Brandt, M.E., Martens, J., Brewer, R.S., et al. (2016b). Potential Structuring Forces on a Shelf Edge Upper Mesophotic Coral Ecosystem in the US Virgin Islands. Front. Mar. Sci., 3. Smith, T.B., Gyory, J., Brandt, M.E., Miller, W.J., Jossart, J. & Nemeth, R.S. (2016c). Caribbean mesophotic coral ecosystems are unlikely climate change refugia. Global Change Biology, 22, 2756–2765. Steneck, R.S., Paris, C.B., Arnold, S.N., Ablan-Lagman, M.C., Alcala, A.C., Butler, M.J., et al. (2009). Thinking and managing outside the box: coalescing connectivity networks to build region-wide resilience in coral reef ecosystems. Coral Reefs, 28, 367–378.

Taylor, J., Cherubin, L., Schärer, M., Michaels, W., Caillouet, R., Campbell, M., et al. (2020). Emerging Science and Technology to Improve Monitoring and Assessments of Fish Spawning Aggregations Report from the 2019 Gulf and Caribbean Fisheries Institute Workshop. The United States Virgin Islands TERRITORIAL CORAL REEF MONITORING PROGRAM Annual Report (Annual Report). (2018). TERRITORIAL CORAL REEF MONITORING PROGRAM. The Center for Marine and Environmental Studies, University of the Virgin Islands, The Division of Coastal Zone Management, USVI Department of Planning and Natural Resources, The Coral Reef Conservation Program, National Oceanic and Atmospheric Administration. Townsend, J. (2019). Lesion recovery of two reef-building coral species across shallow to mesophotic depths. Master of Science in Marine and Environmental Sciences. University of the Virgin Islands, US Virgin Islands. Tuohy, E., Nemeth, M., Bejarano, I., Schärer, M. & Appeldoorn, R. (2015). I>In situ Tagging of Nassau Grouper Epinephelus striatus Using Closed-Circuit Rebreathers at a Spawning Aggregation in Puerto Rico. Marine Technology Society Journal, 49. Weinstein, D., Sharifi, A., Klaus, J., Smith, T., Giri, S. & Helmle, K. (2016). Coral growth, bioerosion, and secondary accretion of living orbicellid corals from mesophotic reefs in the US Virgin Islands. Marine Ecology Progress Series, 559, 45–63. Weinstein, D.K., Klaus, J.S. & Smith, T.B. (2015). Habitat heterogeneity reflected in mesophotic reef sediments. Sedimentary Geology, 329, 177–187. Weinstein, D.K., Smith, T.B. & Klaus, J.S. (2014a). Mesophotic bioerosion: Variability and structural impact on U.S. Virgin Island deep reefs. Geomorphology, Coral Reef Geomorphology, 222, 14–24. Weinstein, D.K., Smith, T.B. & Klaus, J.S. (2014b). Mesophotic bioerosion: Variability and structural impact on U.S. Virgin Island deep reefs. Geomorphology, Coral Reef Geomorphology, 222, 14–24. Williams, L., Smith, T., Burge, C. & Brandt, M. (2020). Species-specific susceptibility to white plague disease in three common Caribbean corals. Coral Reefs, 39. Williams, S.M. & García‐Sais, J.R. (2020). A potential new threat on the coral reefs of Puerto Rico: The recent emergence of Ramicrusta spp. Marine Ecology, 41, e12592. Zayas-Santiago, C.M. (2019). Red hind Epinephelus guttatus vocal repertoire characterization, temporal patterns and call detection with micro accelerometers. Thesis.