The Reef Corridor of the Southwest Gulf of Mexico: Challenges for Its Management and Conservation

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Ocean & Coastal Management 86 (2013) 22e32

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Ocean & Coastal Management

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The Reef Corridor of the Southwest Gulf of Mexico: Challenges for its management and conservation

Leonardo Ortiz-Lozano a,*, Horacio Pérez-España b,c, Alejandro Granados-Barba a, Carlos González-Gándara d, Ana Gutiérrez-Velázquez e, Javier Martos d a Análisis y Síntesis de Zonas Costeras, Instituto de Ciencias Marinas y Pesquerías, Universidad Veracruzana, Av. Hidalgo #617, Col. Río Jamapa 94290, Boca del Río, Veracruz, Mexico b Arrecifes Coralinos, Instituto de Ciencias Marinas y Pesquerías, Universidad Veracruzana, Av. Hidalgo #617, Col. Río Jamapa 94290, Boca del Río, Veracruz, Mexico c Centro de Investigación de Ciencias Ambientales, Universidad Autónoma del Carmen, Av. Laguna de Términos s/n, Col. Renovación 2da sección, CP 24155, Ciudad del Carmen, Campeche, Mexico d Laboratorio de Arrecifes Coralinos, Facultad de Ciencias Biológicas y Agropecuarias, Zona Poza Rica Tuxpan, Universidad Veracruzana, Carr. Tuxpan.- Tampico km 7.5, Col. Universitaria, CP 92860, Tuxpan, Veracruz, Mexico e Posgrado. Instituto de Ecología, A.C., Departamento de Ecología y Comportamiento Animal, Apartado Postal 63, Xalapa 91000, Veracruz, Mexico article info abstract

Article history: Flow of species and spatial continuity of biological processes between geographically separated areas Available online may be achieved using management tools known as Ecological Corridors (EC). In this paper we propose an EC composed of three highly threatened coral reef systems in the Southwest Gulf of Mexico: Sistema Arrecifal Lobos Tuxpan, Sistema Arrecifal Veracruzano and Arrecifes de los Tuxtlas. The proposed EC is supported by the concept of Marine Protected Areas Networks, which highlights the biogeographical and habitat heterogeneity representations as the main criteria to the establishment of this kind of networks. These three reef systems represent the coral biodiversity of the western Gulf of Mexico. Nevertheless there are serious shortcomings in its protection. Under this approach, the challenges that Mexican government will face for management and conservation of this EC are discussed. There is an obvious lack of an adequate legal framework to establish networks of protected areas in Mexico, mainly because national legislation does not consider connectivity as an important factor in the selection of MPA. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction these ecosystems is within a Marine Protected Area (MPA). How- ever, the number of MPAs and its coverage can be misleading in- One of the most important instruments for in situ protection of dicators of effective conservation of coral areas, since its natural resources and biodiversity has been the establishment of establishment does not warrant the application of good manage- protected areas (Ortiz-Lozano et al., 2009a). These areas, under ment measures and enforcement (Mora et al., 2006; Fraga and different categories of protection, are the basis for international Jesús, 2008). efforts to counter the effects of human development on the envi- Although MPAs are intended to limit human activities, coral ronmental goods and services that they provide. reefs are vulnerable to threats from outside the boundaries of the Coral reefs are one of the marine ecosystems that have provided protected area, such as turbidity and sedimentation (Orpin et al., more goods and services to humans. With a total world area of 2004; James et al., 2005), water pollution (Fabricius, 2005), and approximately 527 000 km2 (Mora et al., 2006), coral reefs have coastal development (Fichez et al., 2005; Mora et al., 2006; Ortiz- been intimately linked to human development and have suffered Lozano, 2012)(Gutiérrez-Ruiz et al., 2011; Ortiz-Lozano, 2012). its consequences (Fitzpatrick and Donaldson, 2007; Hoegh- Also, life cycles and ethology of different reef species may exceed Guldberg et al., 2007). That is why about 20% of the global area of the geographical boundaries of protected areas (Palumbi, 2004)as well as internal ecological processes dominated by the inﬂuence of the external areas (McClelland and Valiea, 1998; Miller and Ayre, * Corresponding author. Tel./fax: þ52 229 9567070. 2008), which increases the vulnerability of reefs to the effects of E-mail addresses: [email protected], [email protected] (L. Ortiz-Lozano). anthropogenic impacts.

Fig. 1. Reefs Systems of the Southwest Gulf of Mexico: Sistema Arrecifal Lobos Tuxpan (SALT), Sistema Arrecifal Veracruzano (SAV) and Arrecifes de los Tuxtlas (AT).

For these reasons, it is necessary to analyze MPAs, not only in the establishment of the first Mexican Marine Protected Area terms of individual performance, but in relation to the major re- Network in the Gulf of Mexico. gions that integrate and represent a relevant role in its spatial and temporal permanence (Pressey, 1994; Hansen and Defries, 2007; 2. Reefs of the Gulf of Mexico Ortiz-Lozano et al., 2009a). Ecological corridors (EC) are biological or physical strips con- The Gulf of Mexico is a Large Marine Ecosystem (Sherman, 1991) necting areas and allowing movement of species (Van der Windt with a mixture of ecological characteristics of temperate and and Swart, 2008). EC have become a concept for integrating, un- tropical environments. It is an inland sea whose basin of der a management perspective, areas that despite being 1.5 106 km2 (Bryant et al., 1991) receives discharges from rivers geographically separated from each other, maintain a flow of spe- that led to the formation of environmentally and biologically cies that generates connections between areas within it. diverse coastal systems. The aim of this manuscript is to present the Southwest Gulf of Coral reefs require particular oceanographic and environmental Mexico reefs as a marine ecological corridor. Here we show the conditions such as shallow, oligotrophic, and warm (>20 C) ma- importance of these reefs and the main stressors to which they are rine waters, with an optimum between 26 and 28 C, with salinities exposed. We explain the criteria to account this ecological corridor of 33e36 ups, minimal turbidity and sedimentation, well lit and under the figure of a network of marine protected areas. with low wave energy (Hubbard, 1997; Carricart-Ganivet, 2004). To arrive at this proposal, we conducted a qualitative approach However, in the Gulf of Mexico, some reefs developed despite the at different spatial scales. First, we considered the large region conditions of turbidity, sedimentation, temperature and organic which includes the Gulf of Mexico (GoM). The GoM was divided inputs, produced by natural disturbances and human activities according to their geological characteristics and the presence of (Salas-Pérez and Granados-Barba, 2008; Salas-Pérez and Arenas, reef systems. With this, we identified the factors that group these reef systems into two sets, according to the type of continental shelf, either carbonated or sedimentary. At a smaller spatial scale Table 1 Scleractinean Coral Species in Gulf of Mexico reef areas. for sedimentary platform reefs, we integrate information about the presence of scleractinian coral species, the main environmental Reef system Number of Source coral species characteristics, the relationship with human uses and the pressures to which they are subjected. This information was obtained from Flower Garden Banks 23 Aronson et al., 2005 published data for different reef systems and expert knowledge in Sistema Arrecifal 28 Horta-Puga et al., 2007 Lobos Tuxpan each of the areas. Evidence of connectivity between different reef Sistema Arrecifal 38 Horta-Puga et al., 2007, this research systems was collected from the scientific literature, considering Veracruzano existing data on benthic organisms. We must emphasize that the Arrecifes de Los 20 Pérez-España et al., 2008; CONANP, 2009 main purpose of this paper is to set the conceptual basis to coor- Tuxtlas Banco de Campeche 44 Horta-Puga et al., 2007, this research dinate research efforts and management of this Reef Corridor, and 24 L. Ortiz-Lozano et al. / Ocean & Coastal Management 86 (2013) 22e32

Table 2 (>150 km width). It is one of the few regions in the world showing a Scleractinean Coral Species in the Southwest Gulf of Mexico reef systems. Sistema sedimentary gradient from terrigenous to biogenic materials (car- Arrecifal Lobos Tuxpan (SALT), Sistema Arrecifal Veracruzano (SAV), Arrecifes de Los bonate). Because of these characteristics, reef systems with variable Tuxtlas (AT). The closest reef system, Banco de Campeche reefs (ABC), is included as an external reference. Sources: Horta-Puga et al., 2007; Pérez-España et al., 2008; morphology and development are found (Heilprin, 1890; Lara et al., CONANP, 2009; *Perez-España personal communication. 1992; Carricart-Ganivet and Horta-Puga, 1993; Jordán-Dahlgren,

# Family Species SALT SAV AT ABC 2002). The environmental heterogeneity and biological complexity of 1 Acroporidae Acropora cervicornis 1111 the Gulf of Mexico is reflected in the shelf off the coast of Veracruz, 2 Acropora palmata 1111 w e < 3 Agariciidae Agaricia agaricites 1111 which is narrow ( 6 33 km), shallow ( 70 m) and sinuous, with 4 Agaricia fragilis 1111 complex topography due to the presence of reefs, islands and 5 Agaricia humilis 0111 submarine canyons. According to Salas-Pérez and Granados-Barba 6 Agaricia lamarcki 0101 (2008), physiographic complexity of this region is important in 7 Helioseris cucullata 0111 fl 8 Caryophylliidae Cladocora arbuscula 0011 modifying ows generated by different components of circulation 9 Mussidae Colpophyllia natans 1111 associated with oceanographic conditions in the Gulf of Mexico 10 Diploria clivosa 1111 (hydrographic parameters, oceaneatmosphere interaction and 11 Diploria labyrinthiformis 0001 circulation), supporting retention and survival of reef systems. 12 Diploria strigosa 1111 There are three well-defined areas with different degree of coral 13 Favia fragum 0101 14 Manicina areolata 1101 development within the region (Fig. 1), hosting 40 species of 15 Mussa angulosa 1101 scleractinian corals (Table 2): Sistema Arrecifal Lobos Tuxpan 16 Mycetophyllia aliciae 0001 (SALT), Sistema Arrecifal Veracruzano (SAV) and a set of small reefs 17 Mycetophyllia daniana 1101 called Arrecifes de Los Tuxtlas (AT). There are also patches of sub- 18 Mycetophyllia ferox 1101 19 Mycetophyllia lamarckiana 1101 merged reefs that share species with these main reef systems. 20 Scolymia cubensis 1101 The characteristics of these systems are: 21 Scolymia lacera 0101 22 Meandrinidae Dichocoenia stokesi 0101 3.1. Sistema Arrecifal Lobos Tuxpan (SALT) 23 Eusmilia fatigiata 0001 24 Meandrina meandrites 0001 25 Pocilloporidae Madracis decactis 1111 This system is composed of platform reefs, six of which are 26 Madracis auretenra* 0101 emerged and four are submerged (Fig. 2, Table 3). Because of its 27 Montastraeidae Montastraea annularis 1101 ecological, scientific, educational, recreational, historical and cul- 28 Montastraea cavernosa 1111 tural importance, in June 2009 was declared an MPA with the 29 Montastraea faveolata 1101 category of “Flora and Fauna Protection Area” (DOF, 2009). There is 30 Montastraea franksi 1101 31 Oculinidae Oculina diffusa 1111 a characteristic type of reefs in the region as is pointed out by 32 Oculina robusta 0111 Castro-Aguirre and Márquez-Espinoza (1981), consisting of high 33 Oculina tenella 0011 relief structures that do not reach the sea surface, called “sub- 34 Oculina valenciennesi 0101 merged reefs”. In the intertidal zone off Cabo Rojo, is “Bajo Verde”,a 35 Oculina varicosa 1111 36 Poritidae Porites astreoides 1111 patch of limestone covered by remains of mollusks, polychaete 37 Porites branneri 0101 tubes and with a coral cover less than 5%, formed mainly of stony 38 Porites colonensis 1101 corals (Fig. 2B). There are also two reef structures located west of 39 Porites divaricata 1101 Tuxpan reef, and another located southeast of the mouth of the 40 Porites furcata 1101 Cazones river (Fig. 2B and C). The dimensions of these reefs are 41 Porites porites 1101 e 42 Siderastreidae Siderastrea radians 1111 similar to those emerging reefs, as they are 1.5 2.5 km long by 1 km 43 Siderastrea siderea 1111 wide (Martos, 2010; González-Cobos, 2010). 44 Astrocoeniidae Stephanocoenia intersepta 1111 Although the first formal studies of SALT date back to Moore Total species 28 38 20 44 (1958), knowledge of their biodiversity and their communities is limited. There are 1 110 species known in the area, emphasizing fi 2010; Pérez-España et al., 2012; Tunnell, 1992; Godinez-Ortega corals, mollusks and shes, including 31 species of stony corals (Escobar-Vázquez and Chávez, 2012; Morales, 2012) that provide et al., 2009; Gutiérrez-Ruiz et al., 2011; Ortiz-Lozano, 2012). shelter for 299 mollusk species (Tunnell et al., 2007) and 278 fish In the Gulf of Mexico, reefs are distributed in two major groups species (González-Gándara, 2003, 2010). Limited knowledge of linked to the environmental features of the continental shelf were some taxa, such as sponges and tunicates is highly remarkable. they are located: the terrigenous platform present in West and North, and the Southeastern carbonate platform (Fig. 1). In the 3.1.1. Economic importance terrigenous shelf biological diversity is lower (Tunnell, 1988; The SALT is located near Tuxpan and Tamiahua cities, whose Jordán-Dahlgren, 2002) due to the extreme conditions in which productive activities are linked in part to these reef ecosystems. they develop and the longest distance and low connectivity they fi have with the center of the Caribbean Biogeographic Province; the Signi cant economic incomes arise from port of Tuxpan, which received 585 vessels in 2012, most of them carrying fuel (SCT, carbonated shelf is closer to the Caribbean and have a higher bio- fi logical diversity (Horta-Puga et al., 2007)(Table 1). 2013). About 100 shermen extracted species for regional and national consumption, mainly octopus. Also, domestic tourism for diving and reef fishing is important in the region. 3. Reefs of the Southwest Gulf of Mexico (RSGoM) 3.1.2. Environmental impacts The East Mexico Shelf (Bryant et al., 1991, Fig. 1) is located in the SALT reefs are apparently less exposed to human activities; Southwest Gulf of Mexico. It is a continental shelf with unusual however, the growth of the Port of Tuxpan and accidental fuel topographic features, narrowing from north to south (w90e6km discharges are increasing pressures on coral reefs. Tuxpan river width), and widening to its boundaries with the Yucatan Shelf pollutes with contaminants as biocides, fertilizers, heavy metals L. Ortiz-Lozano et al. / Ocean & Coastal Management 86 (2013) 22e32 25

Fig. 2. The Flora and Fauna Protection Area, Sistema Arrecifal Lobos Tuxpan (A). It is composed by two polygons: B) North polygon, in front of Tamiahua Lagoon. C) South polygon, in front of Tuxpan city. and fecal coliform to the region (Ponce-Velez and Botello, 2005) relevance in the last six years (Taylor and Akins, 2007; Winfield (Table 4). et al., 2007, 2009, 2010; Okolodkov et al., 2007, 2011; Ortiz- Lozano et al., 2007, 2009a, b; Salas-Pérez et al., 2012; Salas-Pérez 3.2. Sistema Arrecifal Veracruzano (SAV) and Granados-Barba, 2008; Okolodkov, 2008, 2010; Godínez- Ortega et al., 2009; Salas-Monreal et al., 2009; Aké-Castillo et al., The SAV is the most developed reef system in the region. It has 2010; Parra-Toriz et al., 2010; Arceo and Granados-Barba, 2010; 27 reefs, and six islands (Fig. 3, Table 5). It has four fringing reefs, Aké-Castillo, 2011; Ortiz-Lozano, 2012Salas-Pérez et al., 2012). It is and the rest are platform reefs. Of these, 19 are emerged and four also the only system in the region adjacent to a metropolitan area are submerged. The SAV has three categories of protection. It has (Veracruz). There are vessels entering to the commercial port been a national park since 1992 and was declared as a Biosphere through the MPA. These aspects are crucial to the impacts and fl Reserve by UNESCO since 2006. Additionally, was registered by the human in uence on SAV (Hayasaka Ramírez, 2011; Ortiz-Lozano, Mexican government as a wetland of international importance in 2012). the Ramsar list in 2004. Until today there is not a management program for the protected area, making it difficult to conduct 3.2.1. Economic importance proper management and conservation actions. The SAV is the most important reef area in the history of Spanish The SAV is the best studied reef system of Southwest Gulf of colonization (Rodríguez and Manrique, 1991). From the late fi Mexico (Jiménez et al., 2007) and has acquired particular scientific sixteenth century has been both a shelter to the rst port in continental America and the source of material for the construction of Table 3 the city of Veracruz. The Port of Veracruz moved 729 717 containers Reefs of the Sistema Arrecifal Lobos Tuxpan. Location, area and types. in 2007 (Guerrero and Rivera, 2009). There are around 500 fishing 0 Reef name Lat. Long. Average surface Reef type families in the area. The value of the catch in 2006 was U.S. $ 1 915, (ha) 047, the value of diving tourism in 2008 was U.S. $ 50444, 774, and 0 Blanquilla 21.533333 97.288056 49.32501 Platform emerged the beach tourism revenue was U.S. $ 9 519, 365 during the same Medio 21.500000 97.237222 32.24406 Platform emerged year (Arceo et al., 2010). Lobos 21.450000 97.220278 199.70091 Platform emerged Tanhuijo 21.133333 97.271111 90.90751 Platform emerged En Medio 21.066667 97.254167 37.23010 Platform emerged 3.2.2. Environmental impacts Tuxpam 21.016667 97.186389 97.90615 Platform emerged SAV reefs are located in a heavily impacted area. There have Cabo Verde 21.553889 97.321944 NA Platform Submerged been identified 17 different types of environmental impacts asso- Oro Verde 21.188889 97.288056 NA Platform Submerged ciated with 50 different causes of both human and natural origin Pantepec 21.045833 97.237222 NA Platform Submerged (Ortiz-Lozano, 2012). While there is no accurate assessment of the Blake 20.758333 96.999722 NA Platform Submerged impacts in the area, it can be said that urban development of the 26 L. Ortiz-Lozano et al. / Ocean & Coastal Management 86 (2013) 22e32

Table 4 Veracruz metropolitan area, and the presence of the Port of Vera- Environmental problems located in the Southwest Gulf of Mexico reefs. Sistema cruz have been responsible for most of the deterioration of the reef Arrecifal Lobos Tuxpan (SALT), Sistema Arrecifal Veracruzano (SAV), Arrecifes de Los conditions (Table 4). Despite being a protected area since August Tuxtlas (AT). Modified from Ortiz-Lozano (2012). 1992, the Mexican federal government, through the Ministry of Category Environmental problem SALT SAV AT Environment and Natural Resources, began in 2011 a legal proce- Direct physical Siltation of coral reef structures X dure to modify the protected area boundaries, excluding a fringing damage to Reef area reduction X X reef called Punta Gorda. This has generated strong social opposi- the reef Rupture and partial XX tion, since the government’s intention is to expand the facilities of fragmentation of corals Coral Death (death, bleaching, XX the Port of Veracruz on the reef area. coral diseases, coral species decline) 3.3. Arrecifes de Los Tuxtlas Destruction of seagrass (direct X physical damage and indirect functional damage This reef system consists of a set of 32 small coral formations off to seagrass beds) the coast of Los Tuxtlas (Fig. 4, Table 6). Most of them formed of Impact on Disappearance of ornamental XX rocky substrates on which different colonies of hard corals species fisheries fish species grow. There is a fringing reef called “La Perla del Golfo”, which Loss of commercial mollusk X reaches 13 km long and 0.5 km wide, and has a coral cover close to species Loss of clam areas (reduction of X 15%, dominated by Diploria clivosa (Pérez-España et al., 2008). The areas suitable for growth whole area is considered within a Marine Protected Area proposal of clams, declining populations called “Arrecifes de Los Tuxtlas”, under the category of Biosphere of clams) fi Reserve (CONANP, 2009). It is an area with a low level of knowledge Decrease in the size of sh XXX fi caught in commercial fishing because it is dif cult to access, and there are only a few records Changes in the Dominance of algae (relative XX about it (Pérez-España et al., 2008). The most complete information structure of increase in the area covered about the area is the technical report that justifies the inclusion of biological by algae) the area as a protected area (CONANP, 2009). It is stressed a coral communities Invasion of exotic species X X species richness similar to that of SALT, although the abundance is Pollution processes Pollution by agrochemical X X Pollution by fecal coliform X X lower. See Table 4 for environmental impacts detected. Pollution from industrial waste X X Pollution generated by oil and XXX 4. Towards the establishment of the Reef Corridor of the petroleum products Southwest Gulf of Mexico Pollution by organic matter X X Heavy metal pollution X X Pollution from solid waste XX Ecological corridors (EC) are strips that connect physical and (trash and other) biological areas that allow movement of species (Van der Windt and Swart, 2008). Although they may be defined in different

Fig. 3. Sistema Arrecifal Veracruzano National Park (A). Include two reef subsystems (Ortiz-Lozano et al., 2009a). B) Veracruz Subsystem. C) Antón Lizardo Subsystem. L. Ortiz-Lozano et al. / Ocean & Coastal Management 86 (2013) 22e32 27

Table 5 Table 6 Reefs of the Sistema Arrecifal Veracruzano. Location, area and types. Location of reefs of Arrecifes de los Tuxtlas (CONANP, 2009).

Reef name Lat. Long. Average surface Reef type Reef name Lat. Long. (ha) Punta Puntilla 18.709667 95.286333 Punta Gorda 19.251085 96.183811 39.02952 Fringing Isla El Terrón 18.701833 95.238833 Galleguilla 19.231271 96.122688 34.98794 Platform emerged La Ensenada 18.704000 95.189833 Blanquilla 19.227298 96.098208 42.48632 Platform emerged Playa Escondida 18.704167 95.185000 Anegada de 19.226322 96.055719 75.84691 Platform emerged La Poza 18.709333 95.157500 Adentro Armita 1 18.686333 95.159833 Verde 19.203466 96.068006 67.11012 Platform emerged Armita 2 18.685167 95.152500 Hornos 19.191584 96.122661 12.02126 Fringing La Herradura 18.681667 95.145500 Pájaros 19.188906 96.089496 113.08381 Platform emerged Playa Hermosa 18.670000 95.126167 Sacriﬁcios 19.177016 96.092385 45.17923 Platform emerged Montepío Costero 18.665833 95.095667 Anegada de 19.158676 95.854501 471.59684 Platform emerged Montepío Poza 18.652833 95.092667 Afuera Punta Sábalo 18.574667 95.082167 Ingenieros 19.149029 96.092824 43.73221 Fringing Muelle Balzapote 18.621833 95.069667 Topatillo 19.142977 95.835755 13.72432 Platform emerged Las Cruces (Punta Balzapote) 18.538000 95.067167 Santiaguillo 19.142477 95.809003 17.50261 Platform emerged Punta Playita 18.609000 95.058167 Anegadilla 19.136971 95.795912 20.62310 Platform emerged Jicacal 1 18.591167 95.037833 Polo 19.108503 95.977635 21.96971 Platform emerged Jicacal 2 18.588500 95.047500 Enmedio 19.106099 95.939164 258.61579 Platform emerged Jicacal Poza 18.621833 95.033333 Los Bajitos 19.101759 95.976463 42.78612 Platform emerged La Playita 18.558167 94.968333 Chopas 19.088364 95.968362 473.62927 Platform emerged Los Morritos 18.557333 94.975667 Blanca 19.086803 95.999618 41.32848 Platform emerged El Salado 18.549667 94.899833 Cabezo 19.074708 95.848202 1037.58564 Platform emerged Los Mulatos 18.552667 94.881833 Giote 19.065980 95.997718 3.45797 Fringing Barco Viejo 18.550000 94.872333 Rizo 19.063957 95.927766 184.40603 Platform emerged Guasinapan 18.548000 94.861167 La Palma 19.12627 95.96835 197.140441 Platform submerged Olapa 18.547500 94.851833 Los Sargazos 19.09851 95.94514 19.2172783 Platform submerged Perla del Golfo 18.525667 94.801833 Periferico 19.08431 95.93388 4.59033383 Platform submerged Zapotitlán 18.514000 94.792667 Terranova 19.18404 96.09553 6.52967079 Platform submerged Mezcalapa 18.468500 94.772000 Sochoapa 18.443500 94.763333 Punta Tecuanapa 18.421667 94.738667 Peña Hermosa 18.357333 94.688167 ways (Good, 1998), the concept itself refers to a particular feature: Punta Peña Hermosa 18.351667 94.674500 connectivity, i.e. communication between two or more entities. El Terrón 1 18.336833 94.658333 This “fuzzy” concept has been accepted by conservationists and El Terrón Poza 18.336667 94.654667 politicians precisely because of its adaptable deﬁnition (Van der Punta San Juan 18.288167 94.620333 Jicacal 18.224333 94.608333 Windt and Swart, 2008). La Cuadrada 18.185333 94.573833 Under an environmental perspective, this connectivity may Palo Seco 18.171667 94.521667 refer to two components: can be related to physical characteristics of the territory that provide connectivity in the landscape, linking core habitats. It can also refer to landscape connectivity, considered a biological attribute, which is the ability of the species (or species assemblages) to disperse over a landscape (Baudry and Merriam,

Fig. 4. Arrecifes de los Tuxtlas. This group of 32 scattered coral formations has been proposed by the Federal Government as a Biosphere Reserve. Dots represent the coral formations. 28 L. Ortiz-Lozano et al. / Ocean & Coastal Management 86 (2013) 22e32

Fig. 7. Dendrogram that shows composition of scleractinian corals species and its distribution in the Southern Gulf of Mexico. Numbers refers to species in Table 2. Here are displayed only 26 of the 44 species of scleractinenan corals. The remaining 18 species are common to all systems. Black dots refer to species shared in each node. White dots represent species shared by ABC and AT. AT ¼ Arrecifes de los Tuxtlas; SALT ¼ Sistema Arrecifal Lobos Tuxpan; SAV ¼ Sistema Arrecifal Veracruzano; ABC ¼ Banco de Campeche Reefs.

The MPAN are appropriate to address space issues of connectivity (e.g. connect sites crucial to certain life stages of key species) and habitat heterogeneity and spatial arrangement and composition of the constituent habitats, all of which contribute to the ecosystem resilience. Fig. 5. NMDS configuration obtained from the polychaete density in selected southern Roberts et al. (2003) proposed several criteria for the selection of ¼ ¼ GoM reefs: CBRS Campeche Bank Reef System, CIRS Cozumel Island Reef System, MPAN, but the most important are: 1) “biogeographic representa- ¼ VRS Veracruz Reef System. VRS includes Lobos (SALT) and Anegada de Adentro and ” “ ” Anegada de Afuera reefs (SAV). (Modified from Granados-Barba et al., 2003). tion and 2) Representation and habitat heterogeneity , because both seek to capture the full spectrum of diversity present in an MPAN. The first one refers to the representativeness of the network 1988). The second is the one that gives greater strength to the of areas to include all biogeographical regions in protected areas of concept. the MPAN, including the transition zones. The second seeks to In terrestrial ecosystems, the EC concept has been criticized protect the full range of habitats present within a biogeographic because of the difficulty to test connectivity between different region. Our proposal is the implementation of an MPAN including areas (Van der Windt and Swart, 2008). However, in marine eco- the reef systems off Veracruz State coast. This MPAN must include systems connectivity is a key factor, especially for benthic organ- the theoretical/best knowledge in order to have representation of isms (Carr et al., 2003). In fact, there are conspicuous physical most habitats and ensure ecological connectivity. drivers that encourage connectivity, such as ocean currents (Brock Bellow we describe how these criteria are applied to the RSGoM. et al., 2012). In reef systems, hydrologic connectivity between their linked environments (mangroves and sea grasses) is critical to complete biological cycles. RSGoM can be seen in the perspective of EC complementing this concept with the criteria for the establishment of Marine Protected Areas Networks (MPAN). These MPAN arise from the need to connect not only interrelated environments, but to unite under common goals the different interests of the social sectors involved in its use and management (Roberts et al., 2003).

Fig. 6. Hierarchical clustering of gorgonian species from South GoM and Caribbean reefs. SALT reefs: Isla Lobos (IL), Tuxpan (TUX); SAV reefs: Veracruz (VER); ABC reefs: Cayo Arenas (AREN), Cayo Arcas (ARC), Triángulos (TRIAN); Caribbean Reefs: Puerto Fig. 8. Types of coral reefs in the Southwest Gulf of Mexico according to its geo- Morelos (PMOR). Modiﬁed from Jordán-Dahlgren (2002). morphology. a) Fringing reefs. b) Emerged platform reefs. c) Submerged platform reefs. L. Ortiz-Lozano et al. / Ocean & Coastal Management 86 (2013) 22e32 29

4.1. Biogeographic representation 4.3. Physical connectivity

Regardless of their hierarchical level, a regional unit is charac- A third issue on the creation of MPAN is the presence of strong terized by the presence of exclusive groups, whose limits are physical connectivity that could favor connectivity between defined by the overlap of the boundary lines of such groups. biological communities. In the case of the Southwestern GoM, However, not all species share the same geographic distribution, there is a remarked connectivity due to continental shelf currents making it difficult to place them in a rigid biogeographic region- (Zavala-Hidalgo et al., 2003). These currents moves northward alization (Zunino and Zullini, 2004). This is the case of the RSGoM. from April to August and southward from September to March, The RSGoM are located at Eastern Continental Shelf of Mexico, allowing the movement of water masses across all the reefs which is within the Wider Caribbean biogeographic province systems of the CE. (Horta-Puga et al., 2007). This Biogeographic province is a vast region stretching from the South American Caribbean to the Gulf of 5. Considerations for the integrated management of the Mexico. Nevertheless, Eastern Continental Shelf of Mexico has its ecological corridor own characteristics, both environmental and benthic species composition, making it different to adjacent areas of the same In Mexico, one of the main tools used by the federal government biogeographic province. for the preservation of marine and coastal resources is the creation Some studies on the geographical distribution of benthic or- of Marine Protected Areas (Ortiz-Lozano et al., 2009a). The General ganisms in the southern Gulf of Mexico and the Caribbean, suggest Law on Ecological Equilibrium and Environmental Protection a separation of the biological communities of the Southwest Gulf of (LGEEPA, Spanish acronym) defines protected areas as the key in- Mexico with respect to the other areas of the same biogeographic strument in the exploitation of natural resources, and assign its province. Granados-Barba et al. (2003), through an analysis of administration to the Ministry of Environment and Natural Re- density of coral reef polychaetes, found that the SAV (Anegada de sources through the National Commission of Natural Protected Adentro and Anegada de Afuera reefs) and SALT reefs (Isla Lobos) Areas. In the RSGoM, there are at least two reef systems that are differ from reefs of Mexican Caribbean and Yucatan platform contained within a marine protected area. The first is the SALT, (Fig. 5). In addition, Jordán-Dahlgren (2002) differentiates gorgo- located in the category of Flora and Fauna Protection Area. This MPA nian coral reefs of Southwest Gulf of Mexico (Tuxpan and Veracruz) is lacking a management program and does not have sufficient staff from those in the Caribbean and Yucatan platform (Fig. 6). to perform the necessary monitoring activities in the area. In the For scleractinian corals, species composition of RSGoM differs from case of PNSAV, has National Park status since 1992, but does not the nearest reef systems, which are located at the Campeche Bank have a management program. Currently the National Park is subject (ABC, Fig.1), located in the Yucatan platform and having greater species to an intense judicial process where the citizens of the region have richness than RSGoM. Both share 39 of 44 species of hard corals (Fig. 7). sued federal authorities to protect the reef system against a port Probably, the low connectivity with Caribbean sea and the expansion project. In the case of AT, there is a proposal to create a different environmental conditions have originated RSGoM’s spe- Biosphere Reserve (CONANP, 2009), although to date no progress cial characteristics, resulting in endemic species in the SAV and has been made in protecting the area. SALT, such as fish Elacatinus jarocho, Elacatinus redimiculus (Taylor Besides these reef systems, there are some reefs that have not and Akins, 2007) and Hypoplectrus castroaguirrei (Del-Moral- been considered in any protection scheme, as is the case of the Flores et al., 2007). Other taxonomic groups with 11 exclusive submerged Blake reef (Fig. 2), which is located near the SALT but is species for the SAV are stomatopod and decapod crustaceans not included in the protected area. described by Winfield et al. (2009), Winfield et al. (2009, 2010; Mexico lacks a legally defined scheme for managing networks of Winfield and Ortiz (2012), and Ortiz et al. (2011). More research protected areas. The closest instrument to this approach is defined is needed on the AT, but this area is likely to share these endemic by LGEEPA as the National System of Protected Areas (NSPA). It is species, which could strengthen the connectivity within the bio- the integration of Natural Protected Areas that are considered of logical corridor. This idea is reinforced by reports of the presence of particular relevance to the country because of its biodiversity and submerged reefs south of SALT (Martos et al., 2009) and north of its ecological characteristics (LGEEPA, 2011). Nevertheless, the SAV, which would reduce the distance between Veracruz reef en- NSPA does not explicitly consider the need to include environ- vironments favoring the idea of an EC. mentally related areas together, or even mention the term Differences between biota belonging to adjacent biogeographic “ecological connectivity”. By contrast, in other countries like the units can be determined by a combination of factors including U.S., there are experiences on the establishment of MPAs networks, unique ecological conditions or barriers to dispersal (biotic or as in the case of the State of California. After the enactment of the physical, current or past) (Cox, 2001; Ruggiero and Ezcurra, 2003) Marine Life Protection Act, the MPAs in the region increased from 3 This higher connectivity among reefs of RSGoM and lower con- to approximately 16% of the State waters. This network of marine nectivity with the Caribbean favor the idea of an biogeographic unit protected areas represents most of marine habitats and is designed that could be seen as an EC (Darlington, 1957). to be ecologically-connected (Gleason et al., 2013). From this perspective, the initiative to create the EC of the 4.2. Representation and habitat heterogeneity RSGoM allows to integrate the term of connectivity within the management of the MPA in the region. One of the main benefits is RSGoM contains all possible types of coral reefs in the Gulf of that considers not only the polygons of protection; it also includes Mexico. Coral reefs can be classified into four types according to the intermediate areas between them. This facilitates the protec- their shape and proximity to the coast (Chávez et al., 2007): atolls, tion of reefs that are not included in any protected areas, but are platform, fringing and barrier. RSGoM has fringing reefs in the SAV equally important for the maintenance of the EC. and the AT, and platform reefs at SALT and SAV. In the systems that The apparent biogeographical ’isolation’ with the rest of the compose the RSGoM, there is a subdivision between platform reefs, Wider Caribbean reef systems, as well as a high physical connec- since platform reefs may emerge from the sea surface or be tivity between CE systems, highlights the vulnerability of the completely submerged (Fig. 8). In addition to these major types of RSGoM. Threats like global warming have been decisive in the loss reefs, in the AT are various patch reefs that grow near the coast. of resilience of reef systems globally (Hoegh-Guldberg et al., 2007), 30 L. Ortiz-Lozano et al. / Ocean & Coastal Management 86 (2013) 22e32 a situation that may be exacerbated in systems with greater the Veracruz Reef System National Park, México: a spatial approach. In: Pro- isolation as RSGoM. ceedings of the Fifteenth Biennial Conference of IFEET. Montpellier, France, pp. 1e10. There are international initiatives that can be used as a frame- Aronson, R.B., Precht, W.F., Murdoch, T.J.T., Robbart, M.L., 2005. Long-term work to develop MPAN management schemes in Mexico. It can be persistence of coral assemblages on the Flower Garden Banks, Northwestern seen either as financing mechanisms or as external regulators to Gulf of Mexico: implications for science and management. Gulf Mexico Sci. 1, 84e94. facilitate the implementation of the commitments made by Mexico Baudry, J., Merriam, G., 1988. Connectivity and connectedness: functional on MPAs. An example of this is the case of the Commission for versus structural patterns in landscapes. In: Schreiber, K.F. (Ed.), Connec- Environmental Cooperation (CEC) resulting from the signing of the tivity in Landscape Ecology, Münstersche Geographische Arbeiten, vol. 29, pp. 23e28. North American Free Trade Agreement (NAFTA) between Mexico, Brock, R.J., Kenchington, E., Martínez-Arroyo, A. (Eds.), 2012. Scientific Guidelines the United States and Canada (1994). The Commission created the. for Designing Resilient Marine Protected Area Networks in a Changing Climate. North American Marine Protected Areas Network (NAMPAN to Commission for Environmental Cooperation, Montreal, Canada, p. 95. Bryant, W., Lugo, J., Córdova, C., Salvador, A., 1991. Physiography and bathymetry. improve and strengthen the conservation of biodiversity in critical In: The Gulf of Mexico Basin. The Geological Society of America ciudad y marine habitats throughout North America MPA and facilitate the páginas. exchange of information between experts and managers (www2. Carr, M.H., Neigel, J.E., Estes, J.A., Andelman, S., Warner, R.R., Largier, J.L., 2003. cec.org/nampan). Comparing marine and terrestrial Ecosystems: Implications for the design of coastal marine reserves. Ecol. Appl. 13, S90eS107. While these initiatives could serve as a catalyst for the estab- Carricart-Ganivet, J.P., 2004. Sea surface temperature and the growth of the West lishment of the Reef Corridor of the Southwest Gulf of Mexico, we Atlantic reef-building coral Montastraea annularis. J. Exp. Mar. Biol. Ecol. 302, e must emphasize the importance local governments can play in this 249 260. Carricart-Ganivet, J.P., Horta-Puga, G., 1993. Arrecifes de coral en México. In: Sala- task. In Mexico, all marine ecosystems are under federal jurisdiction. zar-Vallejo, S.I., González, N.E. (Eds.), Biodiversidad Marina y Costera de México. However, as seen in Fig. 1, the State that borders all the RSGoM is CONABIO - CIQRO, México DF, pp. 81e92. Veracruz. Under the functional perspective of the coastal zone (Ray Castro-Aguirre, J.L., Márquez-Espinoza, A., 1981. Contribución al conocimiento de la ictiofauna de la Isla de Lobos y zonas adyacentes, Veracruz, México. In: Serie and Hayden, 1992; Ortiz-Lozano et al., 2007, 2009a), Veracruz is by Científica, vol. 22. Instituto Nacional de la Pesca, México DF, p. 85. definition the immediate catchment area (or planning zone, in terms Chávez, E.A., Tunnell Jr., J.W., Whithers, K., 2007. Reef Zonation and Ecology: of Sorensen et al., [1992]) for all reef systems that form the EC. Thus Veracruz shelf and Campeche Bank. In: Tunnell Jr., J.W., Chávez, E.A., Whithers, K. (Eds.), Coral Reefs of the Southern Gulf of Mexico. Texas A&M the role of the State and Municipal governments in urban areas is University Press, Corpus-Christi, USA, pp. 41e67. relevant to the management of this MPAN. Therefore, it is necessary CONANP, 2009. Estudio Previo Justificativo para el establecimiento del Área Natural that management of EC is supported by functional schemes to Protegida reserva de la Biósfera “Arrecifes Los Tuxtlas”. Comisión Nacional de Áreas Naturales Protegidas, México, p. 244. Technical Report. Contract SSAP- overcome the jurisdictional limitations and facilitate the inclusion of 2009-86. local governments and territories related with the EC. Cox, C.B., 2001. The biogeographic regions reconsidered. J. Biogeogr. 28, 511e523. The EC would enhance the integration of management initia- Darlington, P.J., 1957. Zoogeography: the Geographical Distribution of Animals. John tives already under way in the area (such as the presence of marine Wiley and Sons, Nueva York. Del-Moral-Flores, L.F., Tello-Musi, J.L., Martínez-Pérez, A., 2007. Descripción de una protected areas and marine ordinances) and would recover the nueva especie del género Hypoplectrus (Actinopterigy: Serranidae) del Sistema concept of environmental connectivity as an essential element in Arrecifal Veracruzano, suroeste del Golfo de México. Rev. Zool. 22, 1e10. the functioning and management of these reef systems in the Gulf DOF, 2009. Decreto por el que se declara área natural protegida, con el carácter de Área de Protección de Flora y Fauna, la región conocida como Sistema Arrecifal of Mexico. Lobos-Tuxpan, localizada frente a las costas de los municipios de Tamiahua y Finally, the approach proposed here, can be useful to highlight Tuxpan, en el Estado de Veracruz. Tomo DCLXIX 5, 79e84. the importance of the transition zones among reef systems Escobar-Vásquez, C., Chávez, E., 2012. Coral community structure at Isla Lobos reef, Gulf of México. Biodiversity and systematic. In: Proceedings of the 12th Inter- considering them as landscape elements that must be addressed as national Coral Reef Symposium, Cairns, Australia, p. 6. they serve as a link between the sites. In addition, the EC proposal Fabricius, K.E., 2005. Effects of terrestrial runoff on the ecology of corals and coral can become the starting point for generating new approaches to the reefs: review and synthesis. Mar. Pollut. Bull. 50, 125e146. Fichez, R., Harris, P.A., Fernández, J.M., Chevillon, C., Badie, C., 2005. Sediment re- study of these reef systems. Under this reasoning, the establish- cords of past anthropogenic environmental changes in a barrier reef lagoon ment of this MPAN can become a valuable tool for the management (Papeete, Tahiti, French Polynesia). Mar. Pollut. Bull. 50, 583e608. of all activities supported on the natural resources of the coastal Fitzpatrick, S.M., Donaldson, T.J., 2007. Anthropogenic impacts to coral reefs in Palau, western Micronesia during the Late Holocene. Coral Reefs 26, 915e930. zone of the state of Veracruz and the Southwest of the Gulf of Fraga, J., Jesús, A., 2008. Samudra monograph: coastal and marine protected areas in Mexico. Mexico. ICSF, India, p. 79. Gleason, M., Fox, E., Ashcraft, S., Vasques, J., Whiteman, E., Serpa, P., Saarman, E., Caldwell, M., Frimodig, A., Miller-Henson, M., Kirlin, J., Ota, B., Pope, E., Acknowledgments Weber, M., Wiseman, K., 2013. Designing a network of marine protected areas in California: achievements, costs, lessons learned, and challenges ahead. Ocean e We thank Patricia Arceo and Gerardo Rios for their help in Coastal Manag 74, 90 101. Godínez-Ortega, J.L., Ramírez-García, P., Pedraza-Venegas, K., 2009. Cambios en la translating this paper. This research was supported by the projects: flora béntica de Arrecife Hornos (Veracruz, México). Rev. Especializada Ciencias “Bases para el Análisis y Síntesis de los Sistemas Costeros de Veracruz, Químico-Biol. 12, 59e65. RASZCOV”; “Sistema Integral de Planeación Ambiental de la Zona González-Cobos, J.M., 2010. Localización y Caracterización de los Arrecifes No ” Emergentes en la costa de Tuxpan, Veracruz. Bachelor thesis. Facultad de Costera Veracruzana UV-ICMP (DGI 32720201023) and GM004 Ciencias Biológicas y Agropecuarias, Universidad Veracruzana, Tuxpan, Vera- “Monitoreo del Sistema Arrecifal Veracruzano” funded by CONABIO. cruz, México, p. 47. 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