Submerged Coral Reefs in the Veracruz Reef System, Mexico, and its implications for marine protected area management

Submerged Coral Reefs in the Veracruz Reef System, Mexico, and its implications for marine protected area management

Ocean and Coastal Management 158 (2018) 11–23 Contents lists available at ScienceDirect Ocean and Coastal Management journal homepage: www.elsevier...

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Ocean and Coastal Management 158 (2018) 11–23

Contents lists available at ScienceDirect

Ocean and Coastal Management journal homepage: www.elsevier.com/locate/ocecoaman

Submerged Coral Reefs in the Veracruz Reef System, Mexico, and its implications for marine protected area management

T

L. Ortiz-Lozanoa, C. Colmenares-Camposb, A. Gutiérrez-Velázquezc,∗ a

Análisis y Síntesis de Zonas Costeras, Instituto de Ciencias Marinas y Pesquerías, Universidad Veracruzana, Mexico Posgrado en Ecología y Pesquerías, Instituto de Ciencias Marinas y Pesquerías, Universidad Veracruzana, Mexico c Instituto Tecnológico de Boca del Río, Mexico b

A R T I C LE I N FO

A B S T R A C T

Keywords: Submerged Coral Reefs MPA management Reef geomorphology Reef stressors

Submerged coral reefs (SCRs) are found on the continental shelves of the tropical regions of the world. Unlike shallow reefs, such submerged structures have been little studied in the world despite their ecological importance. We present the results of several explorations carried out between 2015 and 2017 in the Sistema Arrecifal Veracruzano National Park (SAVNP) and surrounding areas, which account for the presence of 18 SCRs both inside and outside the National Park. The location of these reefs was based on user information, literature and official documents. Through the use of echo sounder, the dimensions and morphological conformation of the reefs were identified. The protection of submerged coral reefs in the SAVPN is limited. They are not fully considered in the MPA creation decrees, and most of them are located in areas assigned to artisanal fisheries. Connectivity, fisheries, port activities and the lack of scientific information are issues to be attended by environmental authorities to guarantee the protection of these ecosystems.

1. Introduction A common theme of successful protected areas established to date is to include, wherever possible, appropriate and available science in the decision-making process (Lundquist and Granek, 2005). In Marine Protected Areas (MPA), effective management may depend, between other issues, in the substantial inclusion of representative habitats (Fox et al., 2012). In the case of MPAs that integrate coral reefs, it is very common for protection and conservation initiatives to focus on those reefs that are near to the surface (Bridge et al., 2013). However, in many cases the spatial distribution and even the existence of deeper reefs are unknown (Harris et al., 2013). In fact, estimates of global impacts on coral ecosystems by anthropogenic activities underestimate the presence of those reefs that are submerged and are not easily detectable (Bridge et al., 2013; Harris et al., 2013). In this paper we present the results of several explorations carried out between 2015 and 2017 in the Sistema Arrecifal Veracruzano National Park (SAVNP), México, and surrounding areas, which account for the presence of Submerged Coral Reefs (SCRs) both inside and outside the National Park. The geographical location and geomorphological configuration of the reefs are shown, and the implications of their presence for the management of the protected area are discussed.



With this work, it is intended that this type of ecosystem be known and considered in the conservation initiatives of the SAVNP, since there is no specific protection policy for its management. 1.1. Submerged Coral Reefs and Mesophotic Coral Ecosystems The Submerged Coral Reefs (SCRs) are found on the continental shelves of the tropical regions of the world, at varying depths ranging from a few meters to more than 150. Due to this, such structures are generally not visible in aerial photographs or satellite images (Harris et al., 2013) nor are they perceptible when navigating the sea surface since they do not present zones of breakage of waves. SCRs are reefs formed during periods of lower sea level, which currently have little or no modern upward coral framework accretion. They are thought to have drowned as a result of inimical environmental conditions associated with sea level rise during the last deglaciation (Abbey and Webster, 2011). Although SCRs have lost their capacity for rapid growth, their ecological importance is notorious. At sites such as the Great Barrier Reef, Australia, these reefs have been reported to substantially increase the availability of suitable habitats for coral growth (Harris et al., 2013), and may contribute significantly to the production of coral larvae (Thomas et al., 2015). In addition, there is a hypothesis that

Corresponding author. Hidalgo 617, Col. Rio jamapa. Boca del Río, Veracruz, Mexico. CP 94290. E-mail address: [email protected] (A. Gutiérrez-Velázquez).

https://doi.org/10.1016/j.ocecoaman.2018.03.012 Received 11 September 2017; Received in revised form 18 January 2018; Accepted 7 March 2018 0964-5691/ © 2018 Elsevier Ltd. All rights reserved.

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Management Program mentions only “drowned” reefs (common name assigned to submerged reefs) but it is not clear to show its location and does not establish particular policies for its protection.

2. Methods The study area is defined as the area between Villa Rica, municipality of Actopan, and Antón Lizardo, Alvarado municipality, both in the state of Veracruz, Mexico (Fig. 2). Explorations were carried out between January 2015 and July 2017 in the study area. The sampling sites were selected from three sources of information. Users. Reports were obtained of fishing sites in the towns of Villa Rica, Chachalacas, Veracruz, Boca del Río and Antón Lizardo. The fishermen provided data on the geographical location of these sites. A SCUBA dive shop in the Port of Veracruz provided us with the geographical coordinates of deep dive sites. Literature. The geographic coordinates of places of interest for the sport diving established in the guide titled “Veracruz and its submarine tourism”, published by the Government of the State of Veracruz, were obtained. Official cartography. Through the National Institute of Access to Information, a bathymetric chart was obtained from the Veracruz Reef System National Park generated in 2015 by the Integral Port Administration of Veracruz (IPA; request 0918200007217). This chart was used to verify the presence of reefs in sites reported by users (fishermen and divers), and to locate other potential reef sites. In addition, cartographic information generated by the National Commission of Protected Natural Areas (NCPNA) was obtained. This information served to locate the polygons of some submerged reefs, which were later modified through the samples made for this research. From these data, visits were made to each site to make a reconnaissance of the place in order to verify the presence of coral structures, regardless of the live coral coverage. Bathymetric data were obtained using an echo sounder GARMIN echoMAP CHIRP 92sv. Since the objective of our research was to locate and demonstrate the presence of submerged reefs, the use of this measurement equipment represents a low cost tool that generates acceptable bathymetric charts. However, the use of higher definition equipment would be advisable for future investigations. Transects were drawn 50 m apart on each submerged structures and depth data were taken every meter. The information collected with echo sounder (coordinates x, y, z) was transferred to a database to be used in the software SURFER 14 (Golden Software). The number of data obtained for each reef was different according to its dimensions (Table 1). Digital models were developed by interpolation (kriging) for each reef. The generated models were exported as isobaths to the ARCGIS software (ESRI) where the polygons of each reef were created. Surface, perimeter and morphological axe were calculated to dimension each reef building. Each identified reef was assigned a name matching the sources of information. If they did not have a name, they were assigned an identification code (Table 2). A review of official documents related to the management of this National Park was made to identify the role of submerged reefs within protection policies, including fishing and port activities. The documents consulted were the Decrees creating the protected area (1992 and 2012) and the Management Program (CONANP, 2017), as well as the Mexican laws related to the subject. In addition, the Environmental Impact Assessment of the Expansion Project of the Port of Veracruz in the North Zone was consulted to identify possible interactions between port activities and SCRs.

Fig. 1. Emerged and submerged reefs and their relationship with the mesophotic zones. A) Submerged reef outside the mesophotic zone; B) emerged reef with windward slope within the mesophotic zone (b); C) Submerged reef within the mesophotic zone.

these types of environments can serve as refuges for species affected by ocean warming (Bongaerts et al., 2010; Bridge et al., 2014; Harris et al., 2013; Riegl and Piller, 2003). Several of these SCRs may represent or contain Mesophotic Coral Ecosystems (MCE). The MCE refer to coral communities that live in areas with low light intensity where photosynthesis is still possible in the zooxanthellae associated with corals (Hinderstein et al., 2010). These areas can have a wide range of depth depending on the particular oceanographic conditions that influence the penetration of solar radiation (Lesser et al., 2009). Not all submerged reefs are mesophotic ecosystems and not all mesophotic ecosystems can be classified as submerged reefs, since the presence of this type of ecosystem is determined primarily by the intensity of the light they receive from the surface. Therefore, many emerged reefs present these mesophotic conditions in their fore reef zone (Fig. 1). 1.2. SCRs in the Gulf of Mexico and Caribbean In the northern portion of the Gulf of Mexico, several SCRs have been discovered, the most prominent and studied being the Flower Banks, which have depths between 36 and 52 m (Parker and Curray, 1956; Moore and Bullis, 1960; Brigth et al., 1984). It is also known the presence of this type of environments in shallow waters on the continental shelf of the Florida peninsula (Rohmann et al., 2005) where MCEs are also presented (Locker et al., 2010). In the Caribbean Sea, the presence of SCRs in the Mesoamerican Reef System has been reported (Bongaerts et al., 2010). Recent studies have found SCR in the Yucatan peninsula (Blanchon et al., 2017), in Utila, Honduras (Andradi-Brown et al., 2016), Dominican Republic (Martínez Battle et al., 2003) and others. 1.3. The Sistema Arrecifal Veracruzano national park The Sistema Arrecifal Veracruzano National Park is a coral reef area located in the central part of the Reef Corridor of the Southwest Gulf of Mexico (RCSGM) (Ortiz-Lozano et al., 2013), being the one that presents/displays a greater number of reef structures and coral species. This Marine Protected Area (MPA) was established by the Mexican Federal Government as National Park since 1992 (DOF, 1992), and acquired the name of Ramsar Site in 2004. Two years later it was registered as a reserve in the UNESCO Man and Biosphere program (Valadéz-Rocha and Ortiz-Lozano, 2013). This National Park underwent a major modification in its protection area in 2012 (DOF, 2012), when its boundaries were changed to facilitate the authorization of the project to expand the Port of Veracruz in Bahía Vergara. After 25 years of lacking a Management Program, in 2017 the Federal Government made official its publication. Despite being a National Park that houses one of the largest Mexican ports, the presence of submerged reefs has been little documented within this protected area. The official charts do not clearly establish the presence of these structures, while fishermen and SCUBA diving service providers are more aware of their presence. The National Park 12

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Fig. 2. Submerged reefs in the Sistema Arrecifal Veracruzano National Park and surrounding areas.

3. Results and discussion

located (Fig. 2). The localization of these reefs was obtained from different sources (Table 2): 16 from users, 1 from literature, 14 from official documents (Integral Port Administration Chart) and only 5 from the National Commission of Protected Natural Areas. Several of the reefs were located based on two or three sources of information. 11

3.1. Submerged reefs In the Sistema Arrecifal Veracruzano, 18 submerged coral reefs were 13

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reefs (North and South) that were separated by an area of seabed without reef structures. In fact, it is in this area where the anchorage zone that is used by the Port of Veracruz is established (Fig. 8). The discovery of these three reefs allows us to appreciate that the two reef areas usually recognized, are not actually separated, but are joined by these structures. It also highlights the presence of SCR outside the MPA in the Northeast region. The reefs 1 and 2 (Figs. 2 and 3) are coral reefs that are far from the protected area (reef 1–33 km and reef 2–7 km). The presence of these structures has not been reported or analyzed in any scientific work or by the environmental authorities of Mexico.

Table 1 Number of data collected with eco sounder for each submerged reef. Code

Reef name

Number of data (XYZ)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Amarillos Monte Negro La Loma Galleguilla N Galleguilla C Galleguilla S Blanquilla N Blanquilla C Blanquilla S Mersey Terranova Pedregales N Pedregales C Pedregales S La Palma Sargazo Periférico Rizo SE

2526 961 2091 3031 3904 6694 12532 9864 7769 3332 5228 7630 8660 8209 42717 23901 3417 11322

3.2. Official protection of the SCR inside the national park The scheme of protected natural areas in Mexico covers different categories. Among them, the National Park is one of the most relevant. According to Mexican Laws, National Parks will be constituted, in the case of biogeographic representations, at a national level, of one or more ecosystems that are signified by their scenic beauty, their scientific, educational, recreational value, their historical value, by the existence of flora and fauna, by its aptitude for the development of tourism, or for other analogous reasons of general interest. In national parks, only activities related to the protection of their natural resources, the increase of their flora and fauna and, in general, the preservation of ecosystems and their elements, as well as research, recreation, tourism and education can be allowed (DOF, 2014). In August of 1992, date of creation of this National Park, little importance was given to the submerged reefs. The delimitation of the boundaries of the MPA was made based only on the emerged and fringing reefs, mentioning 23 structures as conservation objects (18 emerged and 5 fringing reefs). In 2012, a Federal Decree was issued to modify the boundaries of the MPA, where Vergara Bay was excluded, but the boundaries of the National Park were extended to the north, east, and south. This decree mentions for the first time SCR. Five reefs are added to the official list, of which four are submerged and one is a fringing reef. Thus, officially, the Natural Commission of Protected Natural Areas (NCPNA) explicitly recognizes 18 emerged, 6 fringing and 5 submerged reefs. According to the General Law on Ecological Equilibrium and Environmental Protection (LGEEPA by its Spanish acronym; DOF, 2014), which regulates the creation of Protected Natural Areas (PNA) in Mexico, the SAVNP Management Program should have been published in 1992. This happened in May 2017, 25 years later (CONANP, 2017).

SCRs that are inside the MPA are not officially recognized in the decrees of protection of the marine area. In the surrounding area, north of the MPA, two SCR were found (Fig. 2), which are outside the MPA, and therefore are not included in the protection decrees. The total SCR surface is around 595 ha, and a total perimeter of 50.8 km. Of the reefs found inside the SAVNP, the minimum depth was −4 m, while the deepest reached −42 m. The reefs located outside the MPA range from −6 to −26 m. The spatial distribution of the detected SCRs coincides mostly with the emerged reefs, presenting in general an elongated shape with northeast-southwest orientation (Fig. 2). In Figs. 3–7, the bathymetric models of each of the SCRs are presented. The morphological profiles allow to appreciate that in general these reefs have a leeward side with a gentle slope, while the windward side has a steeper slope and reaches greater depths. This form is coincident with that of the emerged reefs from the SAVNP (Lara et al., 1992) although SCRs lack a reef crest. The presence of three SCRs in the central portion of the MPA (reefs 12, 13 and 14, Figs. 2, 5 and 6) is noteworthy, which are located in the bay of the Jamapa River. The previous descriptions of the MPA in scientific studies and in official documents (Krutak et al., 1980; RAMSAR, 2004; MaB UNESCO, 2006; Ortiz-Lozano et al., 2009; CONANP, 2017) considered that the Veracruz Reef System was formed by two groups of

Table 2 Submerged reefs in the Veracruz Reef System National Park and surrounding areas. Localization information (last column) refers to the initial reference obtained to explore these reefs: U: Fishermen and divers; IPA: Integral Port Administration Chart; NCPNA: National Commission of Protected Natural Areas; L: Literature. Code

Reef name

Centroid LAT

Centroid LONG

Area (Ha)

Perimeter (m)

Morphological axis (m)

Topographic axis (m)

Depth min. (m)

Depth max. (m)

Localization information

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Amarillos Monte Negro La Loma Galleguilla N Galleguilla C Galleguilla S Blanquilla N Blanquilla C Blanquilla S Mersey Terranova Pedregales N Pedregales C Pedregales S La Palma Sargazo Periférico Rizo SE

19.537674 19.302556 19.259636 19.262621 19.261842 19.258021 19.254457 19.239295 19.232241 19.18707 19.183929 19.178776 19.169811 19.1694 19.126625 19.099243 19.08329 19.053444

−96.326878 −96.23494 −96.164873 −96.130127 −96.127099 −96.121931 −96.099126 −96.090245 −96.078673 −96.102881 −96.095374 −96.007482 −95.992815 −95.979688 −95.967858 −95.945813 −95.934102 −95.895135

58.269 20.734 29.855 4.50941 7.725286 13.284004 39.438111 35.463 24.076915 3.756248 8.026 20.946 27.823 26.104 162.897604 66.347 5.24177 40.560774

3339.0 1788.0 2622.0 857.9 1143.3 1649.7 3109.9 2843.0 2068.7 1183.0 1468.0 2944.0 2313.0 2437.0 9014.2 7986.0 1211.1 2822.5

608 370 561 194 259 316 537 514 383 124 283 240 559 405 1128 521 166 600

1395 654 645 311 440 634 1258 947 858 438 547 1176 753 907 1754 2100 450 976

−6 −17 −13 −32 −30 −23 −23 −15 −23 −1 −1 −28 −22 −29 −4 −2 −2 −18

−26 −23 −30 −36 −38 −39 −42 −39 −39 −14 −15 −38 −40 −41 −26 −22 −16 −29

U; L U U; IPA U; IPA U; IPA U; IPA U; IPA U; IPA U; IPA NCPNA NCPNA U; IPA U; IPA U; IPA U; IPA; NCPNA U; IPA; NCPNA U; IPA; NCPNA U; IPA

14

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Fig. 3. Bathymetric models and morphological profiles of the Amarillos (1), Montenegro (2), La Loma (3) and Galleguilla N (4) reefs. The red line on the models corresponds to the profiles of each reef. For spatial reference see Fig. 2. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

15

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Fig. 4. Bathymetric models and morphological profiles of the Galleguilla C (5), Galleguilla S (6), Balquilla N (7) and Blanquilla C (8) reefs. The red line on the models corresponds to the profiles of each reef. For spatial reference see Fig. 2. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

16

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Fig. 5. Bathymetric models and morphological profiles of the Blanquilla S (9), Mersey (10), Terranova (11) and Pedregales N (12) reefs. The red line on the models corresponds to the profiles of each reef. For spatial reference see Fig. 2. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

17

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Fig. 6. Bathymetric models and morphological profiles of the Pedregales C (13), Pedregales S (14), La Palma (15) and Sargazo (16) reefs. The red line on the models corresponds to the profiles of each reef. For spatial reference see Fig. 2. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

18

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Fig. 7. Bathymetric models and morphological profiles of the Periferico (17) and Rizo SE (18) reefs. The red line on the models corresponds to the profiles of each reef. For spatial reference see Fig. 2. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

primarily. On the other hand, the Amarillos and Monte Negro reefs (reefs 1 and 2; Fig. 3), being located outside the boundaries of the MPA, are exempt of the associated protection measures, and are used for small-scale fishing. Derived from the above, it is necessary to consider including the SCRs in more stringent protection subzones.

The lack of this Management Program prevented the proper administration of the protected area, which faces several environmental problems (Ortiz-Lozano, 2012). The Natural Protected Areas Management Programs in Mexico are the guiding instrument of planning and regulation that establishes the basic activities, actions and guidelines for the management and administration of these areas. They represent documents where the PNA zoning is proposed, determining the buffer zones and core zones (DOF, 2014). Buffer zones have as their main function to guide the exploitation activities carried out therein towards sustainable development, while at the same time creating the necessary conditions for the conservation of the ecosystems in the long term (DOF, 2014). The core zones have as their main objective the preservation of ecosystems and their functionality in the medium and long term; they can authorize the activities of preservation of ecosystems and their elements, research and scientific collection, environmental education, and limit or prohibit uses that alter ecosystems (DOF, 2014). In the case of the SAVNP, the Management Program refers to the presence of 17 structures not mentioned in the Decree of 2012. However, it does not present the cartography of the reefs and could be assumed to be SCRs. The zoning of the area in the 2012 decree, together with the one in the Management Program, places all the submerged reefs in buffer zones (Fig. 8). There is a sub-zoning for buffer zones, which establishes areas for preservation, traditional use, sustainable use of natural resources and ecosystems, special uses, public use and restoration (DOF, 2014). Only the Sargazos and Periferico SCR (Reefs 16 and 17, Figs. 6 and 7) are assigned to a sub-zone for public use and scuba diving activities. The rest of the SCRs described here are located in areas of sustainable use, which are destined to artisanal fishing activities,

3.3. Implications for management Connectivity. The maintenance of any biological population depends to a great extent on three basic processes: the reproduction capacity of the organisms, the recruitment and the connectivity with other populations at different local and regional scales (SantiagoValentín and Rodríguez-Troncoso, 2016). Self-replication in coral reefs allows the maintenance and growth of local populations due to retention processes, while larval transport to nearby and distant areas favors population connectivity. (Black et al., 1991; Cowen et al., 2003). Connectivity in populations of marine organisms is a relevant issue, since oceanic ecosystems have been considered “open systems”, connected to each other, due to the absence of apparent physical barriers and to the existence of a phase of the cycle vital of organisms dedicated to dispersion (Crooks and Sanjayan, 2006). At present, the study of the connectivity of marine populations has placed particular emphasis on organisms inhabiting coral reefs, because these ecosystems produce a large part of the biomass present in the oceans (Crooks and Sanjayan, 2006). In reef animals (sponges, corals, anemones, crustaceans, fish, etc.), the connection between neighboring subpopulations occurs mainly by larval migration, which is the life stage during which organisms are suspended in water, since they live near the sea floor and move very little in the adult phase, so they are considered relatively sedentary benthic species (Cowen and Sponaugle, 2009). Studies on 19

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Fig. 8. Management sub-zonation of the Sistema Arrecifal Veracruzano national park (CONANP, 2017) and anchoring zones (DOF, 1998; ARGO and APIVER).

represented by at least 89 species (Jimenez-Badillo, 2008). The capture volume presents an annual average of 1343 tons (Dávila-Camacho, 2014). This activity involves the use of boats with outboard motor, and the usual fishing gear are nets, hooks, longlines and in some cases harpoons and hooks. As can be seen in Table 2, it is precisely fishermen who know the location of almost all SCRs. However, to date there are no particular statistics on the actual use made of them. Special policies for the protection of SCR should be reflected in the proposed sub-zoning in the Management Program of the MPA, assigning protection subzones to these environments, as they are currently in areas for small-scale fishing. This is of relevance when considering that it is precisely the fishing activities that have caused a significant loss in the abundance of species of commercial interest in the area (Jimenez-Badillo, 2008; Ortiz-Lozano, 2012). It is noteworthy that fishing for species such as grouper (Epinephelus sp.) on deep reef banks is common, as some species migrate to submerged reefs for spawning (Bridge et al., 2013), and this has been corroborated by fishermen in our area of study. Climate change. Among the main threats facing coral reefs in the world are global climate change and rising ocean temperatures (Anthony et al., 2015). These phenomena, combined with the multiple stressors at the regional and local levels, are one of the fundamental challenges for the management of these ecosystems (Anthony et al., 2015). Derived from this type of pressure, scleractinian corals have suffered the loss of their zooxanthellae colonies, thus causing the whitening events that occur around the world (Brown, 1997). In the case of SAVNP, bleaching events have been documented in several coral genus: Porites (Carricart-Ganivet, 1993), Colpophyllia (Gutiérrez-Ruiz et al., 2011; Carricart-Ganivet et al., 2011), Montastrea (CarricartGanivet et al., 2011), Siderastrea (Carricart-Ganivet et al., 2011) and Acropora (in situ observations). The record of this disease in the SAVPN has been associated to shallow areas, with high solar radiation and high

connectivity from a biogeographic point of view, allow us to determine if the population boundaries are given by physical barriers or by the physiological tolerance that individuals have to disperse (Victor, 1991). The intensity and scale of human disturbances in marine systems are likely to reduce the potential for connectivity between subpopulations due to habitat fragmentation; therefore, the ability of a particular species to cope with threats of extinction will largely depend on its dispersive abilities (Cowen and Sponaugle, 2009). The current problem is that very little is known about the distances of larval dispersion of overexploited, threatened or invasive species; this lack of knowledge makes it difficult to evaluate their connectivity levels, which is a critical aspect both for the design of marine reserve networks and for the development of conservation strategies (Cowen and Sponaugle, 2009). In SCRs from Australia, it has been demonstrated that this type of ecosystem can function as a supplier of coral larvae to emerged and shallow reefs (Thomas et al., 2015). From the perspective of conservation, the presence of SCRs in the SAVNP is of great relevance to understand the functioning and ecological connectivity between the reefs of the area. It could be expected that due to the proximity between reef systems, and that they are subject to the same oceanic conditions, ideal conditions will be generated to form an important connection for the ecosystem functioning of the region (Santiago-Valentín and Rodríguez-Troncoso, 2016). Thus, it is necessary that SAVNP protection policies consider the SCRs in more strict management schemes, which must be accompanied by the necessary scientific studies to evaluate the importance they have in the maintenance of the MPA. Fisheries management. Fishing is one of the most relevant activities in the SAVNP (Jimenez-Badillo, 2008; Arceo et al., 2010; ReynaGonzález et al., 2014). There are at least 1000 fishing families directly dependent on it, and there is an important economic spill associated with the transport and commercialization of fishery products, which are 20

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potential as a tool for ocean governance, further advances in policyrelevant science are required (Fox et al., 2012). Although the science of MPAs is mature and extensive, political discussions are frequently disconnected from that knowledge (Lubchenco and Grorud-Colvert, 2015). The use of scientific knowledge in the management of MPAs that harbor coral reefs remains a great challenge, characterized not only by the limited access of decision makers to academic reports, but also by the lack of effective knowledge transfer schemes for the public policy design (Cvitanovic et al., 2014). In the case of the SCRs, the high degree of ignorance that exists about them in the SAVNP is evident, and even worldwide (Harris et al., 2013). Although SAVNP is an area that has received a lot of attention from the scientific community through different studies (JiménezHernández et al., 2007), research has focused primarily on shallow and emerged reefs. Derived from this lack of knowledge, it is also necessary to understand the importance of these reefs for users who obtain food resources from them or who use them for the development of tourist activities. While the benefits of current protection of unassessed habitats can outweigh delaying conservation implementation until sufficient information is collected (Lundquist and Granek, 2005), there is a need for a balance in the understanding of the ecological and social dimensions of these ecosystems that favor the analysis and design of policies for their management (Christie, 2011).

ocean surface temperatures (Carricart-Ganivet et al., 2011). SCRs in the SAVNP are usually found at depths below the thermocline, which is located between 5 and 10 m depth season related (Avendaño-Alvarez et al., 2017). The stratification of water that occurs markedly in the summer can present differences of up to 4–6 °C between surface waters and those below the thermocline (Salas-Monreal et al., 2009; Avendaño-Alvarez et al., 2017). This situation is relevant, because in places like Indonesia it has been found that the events of coral bleaching associated with high temperatures present a gradient in which the affections decrease as the depth increases (Bridge et al., 2014), which is in agreement with what was found for medium depth reefs (∼20 m) in the Red Sea and South Africa (Riegl and Piller, 2003). In addition, in the Caribbean region it has been found that reefs at depths greater than 30 m are less susceptible to bleaching (Bongaerts et al., 2010). Port activities. The port activity in the SAVNP is intense. The port of Veracruz receives an annual average of 1700 vessels (APIVER, 2018). There are three common environmental impacts in reef zones bordering ports: anchoring damage, coastline modifications and vessel groundings. Damage to coral reefs by vessel anchoring has been widely documented around the world (Beeden et al., 2014; Dinsdale and Harriott, 2004; Davis, 1977) and can cause catastrophic damage in a single event (Smith, 1988) and measures should therefore be taken to avoid this type of damage within the MPA. In this study, it has been found that three reefs (Reefs 12, 13 and 14, Figs. 5 and 6) are adjacent to the anchoring zone used by vessels waiting to enter the port (DOF, 1998) (Fig. 8). This anchorage zone should be analyzed in the light of these findings. Although the reefs that are in that area are located at depths of more than 25 m, the use of anchors can compromise their physical integrity. A similar case may occur with the completion of the Veracruz Port expansion project in the Vergara Bay, since the proposed anchorage zone for this project (ARGO and APIVER), is located between the La Loma and GN, GC and GS reefs (Reefs 3, 4, 5 and 6; Fig. 8). The construction of coastal protection infrastructure is also a point to consider. The influence of this type of activities on shallow reefs has been documented in the SAVPN (Valadéz-Rocha and Ortiz-Lozano, 2013), but the effects on submerged reefs are unknown. Since 2012, a project to expand the Port of Veracruz in Bahía Vergara has begun. However, the environmental impact studies that were carried out to authorize this project omitted the presence of a submerged reef (Reef 3, La Loma, Figs. 1 and 3), which is located 1 km from the breakwaters of the new port. This situation, which was evidenced by groups of local scientists and civil society, prevented the Mexican environmental authority from requesting mitigation measures to reduce impacts on La Loma reef. Vessel groundings on coral reefs reduce the resilience of these ecosystems (Game et al., 2008), and the extent of their impact depends on the reef community structure and on the geomorphology and depth of the site (Connell, 1978, 1997; Hughes, 1989; Karlson and Hurd, 1993). The damages to these ecosystems are mainly caused by vessels making bottom contact, propeller wash, and cable-dragging during salvage and refloating operations (Gittings et al., 1993). Vessel groundings fragment the coral systems and affect the genotypic diversity of a population (Chávez-Romo et al., 2013). Moreover, as these incidents may result in spills of substances into the sea, it is important to investigate them in order to monitor the health of these ecosystems (Piatt and Ford, 1996; Chabanet et al., 2005). According to HayasakaRamirez and Ortiz-Lozano (2014), there is a moderate risk of stranding occurring in the SAVNP, with human errors being the main cause. Within the SCRs located in this study, the La Loma reef, whose minimum depth is 13 m, is the most vulnerable to this type of accident, since it is only 1 km away from the facilities of the new port. That is why it is necessary to consider the presence of this reef in the management of the maritime traffic routes of access to the new port. Scientific Information needs. For MPAs to realize their full

4. Conclusions At the global level, knowledge about SCRs is incipient, a situation that also occurs in the SAVNP. The use of secondary sources of information, such as literature, official documents and the knowledge of users has been an effective tool in locating SCRs in the SAVNP. The protection of submerged reefs in the SAVPN is limited. They are not fully considered in the MPA creation decrees, and most of them are located in areas assigned to artisanal fisheries. There is an urgent need to generate scientific information to adjust the management of the SAVNP to include the SCRs and guarantee the permanence of these ecosystems. Faced with the different stressors that affect the reefs of the SAVNP, it is necessary to adjust the public policies that allow to regulate efficiently the use of these environments. Acknowledgments This research was made possible thanks to the support of fishermen from Chachalacas, Boca del Río, Veracruz and Antón Lizardo. We thank Dorado Buceo diving shop, in Veracruz, for its support for the Bathymetric Surveys, location and recognition of the sites. The Centro Mexicano de Derecho Ambiental A.C. and The Paul M. Angell Family Foundation funded part of this work. The second author receives a grant from the National Council of Science and Technology (CONACyT) scholarship 607761. This research is part of the DGI project: 32720201692 “The Southwest Reef Corridor of the Gulf of Mexico”. References Abbey, E., Webster, J.M., 2011. Submerged Reefs. In Encyclopedia of Modern Coral Reefs. Springer, Netherlands, pp. 1058–1062. Andradi-Brown, D.A., Gress, E., Wright, G., Exton, D.A., Rogers, A.D., 2016. Reef fish community biomass and trophic structure changes across shallow to UpperMesophotic reefs in the Mesoamerican Barrier Reef. Caribb. PloS one 11 (6), e0156641. Anthony, K., Marshall, P.A., Abdulla, A., Beeden, R., Bergh, C., Black, R., Green, A., 2015. Operationalizing resilience for adaptive coral reef management under global environmental change. Glob. Change Biol. 21 (1), 48–61. APIVER (Administración Portuaria Integral de Veracruz), 2018. Resumen histórico, Admnistración Portuaria Integral de Veracruz. http://www.puertodeveracruz.com. mx/estadisticas/resumen-historico/. Arceo, P., Pérez-España, H., Bello, J., Granados-Barba, A., Salas-Monreal, D., OrtízLozano, L., 2010. Economic Evaluation of Fisheries and Tourist Services of the

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