Next Article in Journal
Research Progress on Global Marine Gas Hydrate Resistivity Logging and Electrical Property Experiments
Next Article in Special Issue
Assessment of the Vulnerability of the Lucana Coastal Zones (South Italy) to Natural Hazards
Previous Article in Journal
Filtration Rates and Scaling in Demosponges
 
 
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

A Review of Disturbances to the Ecosystems of the Mexican Caribbean, Their Causes and Consequences

1
Instituto de Ingeniería, Universidad Nacional Autónoma de México, Mexico City 04510, Mexico
2
Ambiente y Sustentabilidad, Instituto de Ecología, A.C., Xalapa 91073, Mexico
3
Unidad Académica de Sistemas Arrecifales, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Puerto Morelos 77580, Mexico
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2022, 10(5), 644; https://doi.org/10.3390/jmse10050644
Received: 10 March 2022 / Revised: 23 April 2022 / Accepted: 4 May 2022 / Published: 9 May 2022
(This article belongs to the Special Issue Natural and Human Impacts in Coastal Areas)

Abstract

:
In a relatively short timescale (less than 50 years), urbanization has caused many anthropogenic disturbances that have affected ecosystem health and, directly or indirectly, quality of life for the local human population. Global disturbances, such as climate change, can also have a substantial, overarching impact on ecosystems. In this scenario, natural disturbances, previously considered an integral part of ecosystem dynamics, can now cause irreversible change to the state of ecosystems, and at the same time, negatively impact social and economic systems. The objective of this study was to identify ecosystem disturbances at a site of interest to recommend strategies to improve coastal zone management. We chose the Mexican Caribbean as a case study, because its biological and cultural complexity render it an interesting location from a coastal management point of view. The PRISMA framework was used to conduct a systematic literature review to identify the ecosystem disturbances that affect this area, as well as the main causes and consequences of these disturbances. Additionally, we discuss how disturbances and their impacts, as screened through PRISMA, can be incorporated into a coastal zone management framework. Results need to consider the limitations associated with using this technique e.g., the degree of impact from a current disturbance may vary from that reported in an earlier publication. Despite its limitations, we believe that this methodology proves useful for identifying key ecosystem disturbances and their consequences, providing a useful tool for identifying appropriate actions to inform coastal zone management plans.

1. Introduction

Environmental degradation is a problem of global concern with potentially irreversible negative socioeconomic and biophysical consequences [1]. At present, one of the main drivers of ecosystem degradation is anthropogenic disturbance [2]. Due to the abundance of the literature on disturbances, different definitions of the term abound [3]. A broad discussion on the topic of disturbances was provided by Battisti et al. [4], although White and Pickett’s definition [5] is still widely accepted today [2,6,7].
Here, as per White and Pickett [5], we took disturbance to be any discrete event in time and space that disrupts the structure of an ecosystem, community, or population and exerts change over resources, substrate availability, or the physical environment.
Disturbances may be classified in several ways depending on the criteria used. Classification into natural or anthropogenic disturbances depends upon the nature of the triggering agent. Natural disturbances are events not induced by human activities, whereas anthropogenic disturbances are those directly, or indirectly, caused by human actions [4]. Another criterion for classifying disturbances is its relative location, with the disturbance being endogenous if it is internal to the system under study or exogenous if it is external [4].
Natural disturbances are critical events that shape ecological systems such as tropical rain forests or coral reefs [8]. In the “state balance” theories of ecosystems, disturbances are the fundamental drivers of spatial and temporal heterogeneity of systems (Figure 1) [2,9]. The internal organization and functions (integrity) of an ecosystem are altered after a disturbance. Depending on the characteristics of the ecosystem and the disturbances affecting them, ecosystems can follow different trajectories in returning to a state of balance or equilibrium [9]. If ecosystem integrity is maintained, the system will return to a state similar to how it was prior to the disturbance; otherwise, a regime shift changing it to a different state will occur [10]. In recent decades, anthropogenic disturbances (e.g., change in land use, pollution, or the introduction of invasive species) and disturbances related to climate change, which also originated from impacts of anthropogenic activities, have increased in frequency, size, and intensity, potentially preventing recovery or adaptive responses on the part of the species that form part of the affected ecosystem [4,6,11]. When these species are unable to recover or adapt to a new biophysical environment, then their survival is threatened, putting at risk the stability of the populations and communities that form the affected ecosystem [4]. A reduction in ecosystem complexity (which is related to the diversity of the organisms of which it is comprised) can negatively modify its resilience (or capacity to reorganize, while undergoing change [12]) to subsequent disturbances [13].
Ecosystems are exposed to multiple disturbances. The set of disturbances that affects a system on a particular scale of time and space is referred to as a disturbance regime [14]. Multiple disturbances can interact and cause unexpected changes in the state of an ecosystem once pushed beyond a critical (or tipping) point (Figure 1) [15]. Hence, disturbances may modify the natural or socio-ecological state of a system, implying a possible reduction in the ecosystem’s natural capital in terms of its essential products and services [4,16]. Improving the understanding of the causes and consequences of disturbances is crucial to the planning of strategies that promote human well-being and the health of ecosystems, providing important information to resource managers and policymakers alike [2,6].
This work aimed to determine the set of characteristic disturbances affecting a study site of interest and to present suitable strategies for use in coastal zone management. The case study was set in the Mexican Caribbean where the Caribbean Sea borders the Mexican state of Quintana Roo. Inland, this area is part of the Mesoamerican region, one of the world’s most biodiverse regions [17] including the “Selva Maya”, the second-largest tropical forest massif in America [18]. The Mexican Caribbean coastline and sea are part of the Caribbean region, one of the global hotspots of marine life (both in the nearshore coastal area and in the open sea) [19]. The Caribbean is also one of the four regions that suffer some of the greatest human impacts worldwide due to overexploitation, habitat destruction, pollution, and climate change [19] with mass tourism adding to the high impact activities in the region [20]. The high cultural and biological diversity of the Mexican Caribbean renders this an area of great importance from a management perspective, also making it an interesting case study.

2. Materials and Methods

A systematic literature review was conducted to identify disturbance events in the key ecosystems of the Mexican Caribbean, of disturbances of the study area. Publications from indexed scientific journals were consulted using the PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analyses) framework [21]. The search was carried out using the Scopus and Web of Science databases. Since the Mexican Caribbean borders the whole length of the Mexican state of Quintana Roo, the words “Quintana Roo” or “Mexican Caribbean” were used to search within the publications’ titles, abstracts, and keywords. The search was limited to papers published prior to 2021 and was carried out between 1 April 2020 and 31 January 2021.

2.1. Inclusion and Exclusion Criteria

We included publications covering events that caused alterations with the potential to destabilize the state of the ecosystem plus those that specifically mentioned actual disturbances. Repeat publications were eliminated, as were those where the location of interest was merely mentioned as the host site of a conference, convention, etc.

2.2. Quality Assessment and Data Extraction

In the search for eligible publications, the first criterion for review was the publication’s title followed by the abstract and the body of the text. I.G. and J.R. reviewed the documents, and any disagreement was resolved by consensus.
For each of the disturbances found in the selected publications, the type of disturbance, the ecosystem involved, and the area in which they occurred were identified to evaluate the following: the amount of disturbance caused by natural phenomena and/or by human activities, the amount of disturbance to the different ecosystems, as well as the municipalities that suffered the greatest number of disturbances, respectively. In addition, to provide a temporal context for the disturbance, the year in which the disturbance occurred was also reported. The disturbances were categorized as either anthropogenic or natural; however, despite the fact that it is known that human activities can cause climate change, this disturbance was placed in its own separate category. This is because, in most documents, the consequences of disturbances are considered future predictions. It is essential to mention that disturbances can be caused by multiple agents; however, this point is rarely addressed. In this analysis, disturbance types (i.e., natural, anthropogenic, or climate change) were counted in isolation of each other. The documents reviewed also used different spatial scales (from local to regional). As the state of Quintana Roo has 11 municipalities (political divisions), disturbances were categorized by municipality so as to maintain a homogeneous spatial scale. In local studies, disturbances were counted as being within the municipality of the study area, whereas in regional studies, disturbances were categorized as pertaining to all of the corresponding municipalities. Table S1 (in the Supplementary Materials section) provides a synthesis of the data gathered. Finally, data relating to the impacts of disturbances on the main ecosystems of the region (tropical rainforest, cenotes, underground cave systems, mangroves, dunes, seagrass meadows, and coral reefs) was collected, as well as the agents triggering these disturbances. In the results section “main causes and consequences of disturbances”, up to three references per disturbance have been cited; however, in Table S1 the complete list of references has been provided per disturbance.

2.3. Characteristics of Qualifying Studies

A total of 1759 publications were collected. Of these, 413 records were found only in Scopus, 327 records were found only in the Web of Science, and 1019 records were found in both databases. Of the 1759 records, 72 publications were eliminated for not meeting the inclusion criteria. Of the remaining 1687 publications, 124 publications met all of the inclusion criteria (Figure 2).

3. Results

3.1. The Mexican Caribbean as a Case Study

The Mexican Caribbean borders the state of Quintana Roo, located on the eastern coast of the Yucatan Peninsula (Figure 3). The climate is warm, subhumid, with average annual temperature ranging from 23 °C to 28 °C and an average annual rainfall of between 700 mm and 1500 mm [22]. February to April tend to be drier months, with the greatest rainfall occurring between May and October. From November to February the area experiences “northerlies”, cold fronts with strong northerly winds [22].
The Yucatan Peninsula has an extensive underground aquifer formed by the infiltration of rainwater through the porous and fractured limestone rock [23]. The network of underground flooded caves of the Yucatan Peninsula was mainly formed by the karst properties of the geological platform and is also believed to have been shaped by the Chicxulub meteorite impact of 65 million years ago [24]. This network of flooded caves is a complex system made up of cavities and interconnected hydrological conduits embedded in the karst aquifer [24,25]. Groundwater movement through the cave systems is considered to be like that of “underground rivers” [26]. Groundwater velocities through the well-integrated flooded cave networks range from 0.5 to 2.5 km/day [26]. There are no surface rivers in the region, hence the water accumulated in the basin is transported directly through the underground cave system. Typical features of the region are cenotes, or sinkholes, i.e., pools of water that connect the surface with the groundwater system and are home to several endemic species [26,27]. The freshwater in this underground system connects to the sea, where it is discharged by means of, what is known locally as, blue holes or “ojos de agua” [28].
The coral reef in the Mexican Caribbean Sea forms part of the Mesoamerican Reef (MAR), the second-largest reef system in the world. The reef system is highly integrated from an ecological perspective [31]. The MAR extends for approximately 1000 km, from north to south, along the Caribbean coastline of Mexico, Belize, Guatemala, and Honduras. The Mexican coastline is 865 km long, hosting 300 km of coral reef [32]. The beaches are mainly sandy, with a small number of rocky shores without cliffs [22]. A variety of habitats are found in the littoral zone, including mangroves, dunes, coastal and reef lagoons, seagrass meadows, and coral reefs. Energy and matter are in constant flux within and between these coastal ecosystems, the adjacent tropical rainforest, and the inland underground water systems, thus the function and health of these ecosystems are closely related to biophysical processes [33].
Over the past five decades, the Mexican Caribbean coast has been the site of almost continuous economic development. The main economic activity in the area is tourism, representing >70% of the GDP in the state of Quintana Roo [20,34]. Throughout the 1980s and 1990s, Cancun, in the north, was the first location in this region to be developed as a tourist resort, now home to a massive hotel infrastructure. Development then spread along the coast to Playa del Carmen, and over to the islands of Isla Mujeres and Cozumel. Tourism requires services, which, in turn, gives rise to domestic migration and triggers fast-paced urban growth [35].

3.2. Disturbances in the Mexican Caribbean

From the literature analysis, 56 disturbances were identified in the various ecosystems, reported in 210 accounts. Reports of disturbances in the literature have increased year by year, starting out with 3 reports in 1991 and reaching 20 reports in 2020 (Figure 4a). Human activity (e.g., urban growth, tourism, or agriculture) caused 67.1% of the disturbances, 12.9% of disturbances were associated with climate change (e.g., sea-level rise, acidification, and increased temperatures), while the remaining 20% were due to large-scale natural phenomena (e.g., hurricanes; Figure 4b). The proportion of each type of reported disturbance varied, depending on the location (Figure 5). The municipality of José María Morelos had the fewest reports (19 disturbances), whilst Tulum was found to have the most (88 disturbances). Table 1 shows the main disturbances reported in the Mexican Caribbean per ecosystem and disturbance event, as well as the type/source of the disturbance based on the following categories: anthropogenic activities, climate change, or whether it was due to a natural phenomenon.

3.3. Main Causes and Consequences of Disturbances

Urban growth and (mass) tourism, as well as activities resulting from them, make up the main causes of anthropogenic disturbances. Meanwhile, the natural disturbances of greatest magnitude in the study area were due to hurricanes and the mass arrival of the seaweed sargassum to the shoreline. Global warming, sea-level rise, and ocean acidification are disturbances associated with climate change that severely impact ecosystems. The following is an overview of the disturbances that occur in the study area by ecosystem, including their impacts and agents.

3.3.1. Rainforest

Damage to this ecosystem is mainly caused by human activity. Urban growth [18,36,37], clearing of forest for agricultural grounds [18,38,39], and fires are the main reported causes of rainforest ecosystem damage (Figure 6) [40,41,42]. Ellis et al. [39] estimated that in southern Quintana Roo, the rate of deforestation from 2001 to 2018 was just over 18%, with agriculture and cattle ranching listed as the main causes. Additionally, Andrade-Herrera et al. [43] reported organochlorine compounds (OCPs) in agricultural soils and conservation areas near agricultural communities in Quintana Roo. The construction of buildings and roads causes displacement and wildlife mortality [44].
Anthropogenic factors include the introduction of exotic species and the extraction of native species. Urbanization sometimes results in the introduction of domestic animals, such as cats and dogs, preying on wild animals in the forest [44,45]. The presence of exotic and invasive fauna has also been documented, including the African honey bee (Apis mellifera) [46], the boa (Boa constrictor) on Cozumel Island [47,48,49], the greenhouse frog (Eleutherodactylus planirostris) [50], the tarantula (Brachypelma vagans) on Cozumel Island [51], the mosquito (Aedes albopictus) [52], the tricolored capuchin (Lonchura malacca) [53], the rock pigeon (Columba livia) [54], the turtle dove (Streptopelia decaocto) [54], the millipede (Cylindrodesmus hirsutus) [55], and the Anolis lizard (Anolis sagrei) [56]. Likewise, exotic flora have been documented (Catharanthus roseus, Corchorus siliquosus, Erechtites hieraciifolius, Leonurus japonicus, Maranta gibba, Mimosa pudica, Phragmites australis, Portulaca oleracea, Pseudogynoxys chenopodioides, Solanum americanum, and Tribulus cistoides), as have shrubs (Solanum erianthum), trees (Citrus aurantifolia), and epiphytes (Nephrolepis multiflora) [57]. The logging of trees and shrubs for wood for commercial and domestic use (e.g., Thrinax radiata palm), as well as the illegal hunting of wildlife (e.g., deer, howler and spider monkeys, or jaguars) may affect biodiversity with cascading impacts [45,58].
Natural disturbances include hurricanes, and in the last 65 years, 43 category 4 hurricanes on the Saffir–Simpson scale and 13 category 5 hurricanes were recorded in the Mexican Caribbean, of which 9 made landfall [59]. Very high-intensity tropical meteorological disturbances are infrequent, but when they do occur, they can have important impacts on rainforest ecosystems. High-intensity hurricanes generate winds with the capacity to knock down trees and reduce the tree canopy, thereby are disturbances with the potential to impact forest dynamics [42,60,61]. The accumulation of organic matter following a hurricane may increase the probability of the spread of fires [41]. In addition to physical damage to vegetation, hurricanes were associated with a decrease in seedling recruitment success of mahogany (Swietenia macrophylla) [61], a species of commercial importance, and an increase in the populations of harmful insects [60].
Climate change also affects forest ecosystems. Garza-López [62] noted that rising temperatures and changes in the length of periods of drought and precipitation could cause the loss of habitat for mahogany (Swietenia macrophylla), an emblematic and commercially valuable species in the region. Heénaut et al. [63] studied associations between bromeliads, spiders, and ants and found that these interactions are governed by periods of flooding and drought, thus it is likely that climate change could affect this biotic association.

3.3.2. Cenotes and the Underground Cave System

Cenotes are an integral part of the network of flooded underground caves connected by conduits [23]. In this system, pollution is the most frequent disturbance. The porosity that gives rise to the aquifer also makes it susceptible to contamination, as pollutants infiltrate the ground surface, reaching the groundwater [64]. Depending upon groundwater velocity, and the connectivity of the below ground conduits, contaminants may be dispersed throughout the network of underground caves (Figure 6) [24], eventually reaching the sea [20].
Groundwater contamination is mainly associated with urban areas [65], agricultural areas [26,66], or roads [26,64]. Compounds that often contaminate groundwater include heavy metals, polyaromatic hydrocarbon compounds, fertilizers, pesticides, or organic matter [64,67,68]. Inadequate disposal of sargassum waste can also potentially affect the water quality of the underground cave system. Chávez et al. [69] noted that leachates from sargassum that have been inappropriately disposed of on land are likely to reach the groundwater due to the high permeability of the soil.
Some cenotes are popular tourist attractions with large numbers of visitors generating local water pollution (e.g., sunscreen residues in the water and inadequate handling of solid waste) [70]. This is particularly relevant given that the underground caves are home to many endemic species [27].
Sea-level rise due to climate change is predicted to be a cause of change in these systems. The below-ground water bodies consist of an upper thin lens of freshwater, recharged by rainwater, which flows towards the coast [65]. The lower, much thicker, layer is saltwater [65]. Sea water intrusion into the aquifer is related to hydraulic conductivity, aquifer recharge, and sea-level rise [25]. Aquifer recharge is compromised by water extraction for increasing human needs, as tourism and populations continue to grow, promoting saline intrusion [24,25,65]. In the Yucatan Peninsula, the underground system is the only source of freshwater [20], and under a sea-level rise scenario, surface seawater and saltwater lenses are projected to move [71] for tens of metres to kilometres inland [25].

3.3.3. Mangroves

Logging and mangrove destruction to make way for housing, infrastructure, and tourist resorts are the main causes of mangrove loss (Figure 6) [72]. The extraction of raw materials [45,72], and the dumping and burning of household waste [37], have put greater pressure on these ecosystems. Hirales-Cota et al. [72] noted that mangroves were being lost in southern Quintana Roo at an annual rate of 0.85% (from 1995 to 2010). Recently, coastal infrastructure in this area has been developing rapidly; so these figures are likely to have increased.
The introduction of exotic species is also affecting the mangrove ecosystem. The invasive species Casuarina equisetifolia (Australian pine) [45] has been reported to be present in large areas with mangrove trees. Domestic animals have also been reported to displace native species; e.g., dogs and feral cats have been observed eating turtle eggs [45].
Like forests, mangroves suffer from defoliation during hurricanes [72]. A 1 m rise in sea level could cause the loss of at least 27% of the mangrove cover in the Mexican Caribbean [73]. The groundwater flows close to the surface in the mangrove zone, and high concentrations of nitrogen compounds, phosphorus, and coliform bacteria associated with contaminated groundwater discharge have been reported in the mangroves [67].
Massive nearshore build-up of sargassum have caused foliage loss due to anoxia. Additionally, large amounts of sargassum have been dumped in many mangrove areas during the clean-up activities that follow massive arrivals of this seaweed [69].

3.3.4. Dunes and Beaches

Dunes occupy 4981 hectares in Quintana Roo, of which 77.3% are in a natural state [74]. As the dunes and beaches are found at the land–water transition, disturbances from both the sea and the land often affect them. Building infrastructure, mainly hotels, on the dune is a problem in several locations in the Mexican Caribbean, especially in the north of the state, where mass tourist infrastructure is highly concentrated (Figure 6) [75,76,77]. Infrastructure built directly on the dune results in sediment loss, which leads to coastal erosion [75,78]. This disturbance has been compensated by artificial (and at times poorly planned) beach replenishment of tourist beaches [76]. Hurricanes have aggravated the erosion induced by humans. In Cancun, Martell et al. [79] noted that after Hurricane Wilma in 2005, 8 million m3 of beach sediment was lost, while Martell-Dubois et al. [76] reported the loss of 31 m of beach after Hurricane Dean in 2007.
Climate change poses a threat to dune-dwelling biota. In addition to the increase in hurricane frequency or intensity, which is expected as a consequence of climate change, increases in solar radiation, temperature, and sea level could affect the fitness of some species. Santo et al. [80] pointed to a decrease in the hatching success of sea turtles, linked to the increase in sand temperature, as well as possible negative impacts on turtle nests as a consequence of increased flooding.
Anthropogenic activities such as mechanical beach cleaning, the removal of organic matter, excessive noise, and the use of beach furniture and lighting on tourist beaches are important disturbances to the beach habitat and its biota [81,82]. Ocaña et al. [81] reported repercussions to sea turtle health (Caretta caretta and Chelonia mydas), while Oliver et al. [82] showed similar findings for the ghost crab (Ocypode quadrata) as a result of these disturbances. The clearing of dune vegetation is common practice on tourist beaches. In addition to disturbing the habitat of native species, clearing facilitates the invasion of non-native species such as the Australian pine [45]. Wild species are also vulnerable to predation by domestic animals in dune areas [45].
Contaminants carried by groundwater can also alter dune conditions by increasing the nutrient load of the substrate. Nitrogen compounds, phosphorus, and coliform bacteria related to contaminated groundwater have also been reported in the dune zone [67,83].
The massive influx of sargassum results in excessive accumulation of this seaweed on the dune. Its decomposition causes an unpleasant smell, beach erosion, and changes in soil characteristics [69]. Erosion is mainly caused by the beach cleaning processes and also due to the loss of the seagrasses that stabilize the substrate through their roots [69].

3.3.5. Marine Water Bodies

Until a few decades ago, the waters of the Mexican Caribbean were characterized as oligotrophic [84]. However, since then water pollution (including human-induced eutrophication) have been reported in coastal lagoons [85,86,87] (Figure 6). Pollution and eutrophication decrease water quality and clarity, affecting the biota that inhabit marine ecosystems [88]. Groundwater flows from cave systems on the mainland discharge pollutants into the sea through submarine springs [87]. Consequently, the highest concentrations of contaminants are usually detected close to these submarine springs [67]. The pollutants and organic compounds discharged directly into the sea are mainly associated with sewerage discharges [89,90,91]. In Quintana Roo, many villages and towns lack water treatment plants, or do not have the capacity to process all the wastewater from the urban populations and the tourist developments [23,87,91]. Metcalfe et al. [26] noted that only 32% of inhabitants have access to a wastewater treatment system. Large resorts often use deep injection wells to pump their wastewater into the aquifer [87]. In addition, effluents from agriculture and industry (fertilizers, pesticides, and other pollutants) have been reported as sources of groundwater and seawater pollution [92,93,94].
Episodes of mass influx of sargassum (Sargassum fluitans and Sargassum natans) to the Mexican Caribbean coastline, which have been recurrent since 2014, have altered seawater properties in the nearshore areas. Several studies have reported an increase in the concentration of nutrients in seawater [69,95,96]. In 2015, a sargassum influx severely affected the northern Mexican Caribbean coast, causing a 15 to 35 fold increase in nearshore sediment, a 3 to 10 fold increase in phosphorus, and a 30 fold increase in nitrogen, while the light extinction Kd increased from 0.26 to 0.37 on average throughout the lagoon [97]. In nearshore waters, sargassum decomposition decreased water pH by up to 1.3 units and increased temperature by up to 2 °C [95]. In the southern Mexican Caribbean, dissolved oxygen decreased from 7.9 mg L−1 to values close to 1 mg L−1 [95].

3.3.6. Seagrass Meadows

Over the last 30 years, due to mass tourism and urban development in the coastal zone, the nutrient content in the seagrass habitat in coastal and reef lagoons has increased [98,99,100]. In the north of Quintana Roo, the land-locked Nichupté Lagoon system, surrounded by the hotel zone of Cancun, is highly eutrophic [85,101,102] and polluted (e.g., by heavy metals) [103]. Seagrasses are the indicators par excellence of increased nutrients in the environment. Van Tussenbroek et al. [102] and Camacho-Cruz et al. [104] found that Thalassia testudinum seagrass had higher amounts of tissue nitrogen content at sites near tourist developments than at sites with less tourist development. The reef lagoons along the coast also received increased amounts of nutrients and other contaminant inputs from groundwater discharges through “ojos de agua”, or submarine springs [91,101], and showed clear indications of eutrophication [105]. Even in these well-flushed reef lagoons, the constant nutrient supply has induced changes in the seagrass community composition as well as in biomass [106,107,108].
The increasing supply of nutrients has caused an increase in phytoplankton and macroalgae [104,109]. Tourist activity can also cause local damage to seagrass meadows directly, through intense snorkelling activities (causing resuspension of sediments) [110] and the anchoring of tourist boats [109].
Major meteorological events, such as hurricanes or tropical storms (e.g., [108,111]), as well as turtle grazing can cause significant damage to seagrass meadows. Seagrass meadows in Quintana Roo have been resilient, showing recovery in the face of these disturbances when anthropogenic disturbances have been absent or negligible (e.g., [111,112] for turtle grazing; [108] for hurricanes or storms). At Akumal, intense grazing by green turtles affected 45 to 55% of a small seagrass meadow, inducing a shift in the seagrass community towards less robust and faster-growing species [111]. While in Puerto Morelos, rotational grazing allowed for full recovery of grazed patches, with a reduced leaf production of T. testudinum from 3.09 to 0.93 g dry wt m−2 d−1 in the grazed patches [111]. However, if not overgrazed, seagrass beds recover gradually, several years after grazing has stopped [111,112]. Hurricanes or storms cause damage to seagrass, including defoliation, detachment of parts, mortality, burial, sediment removal, and exposure of the underground sections of the plants [113,114]. The impact of these events seems to be species-specific; for example, the seagrass Syringodium filiforme was more susceptible to removal and burial by sand than the robust Thalassia testudinum [114,115]. The impacts of hurricanes are not merely associated with physical damage: for example, Hurricane Wilma (a category 4 hurricane that lasted ≈ 3 d) caused drastic temperature changes for a short period, altering the reproductive cycles of seagrasses and seaweeds [116]. On the other hand, Whelan et al. [103] reported the positive effects of Hurricane Wilma on T. testudinum: the heavy metal content in contaminated grasses in the Nichupté Lagoon System fell (probably through the increased flushing of the lagoon) whilst iron content increased in the Puerto Morelos reef lagoon (probably as a result of upwelling).
No reports of changing marine conditions due to climate change were found for the Mexican Caribbean seagrass meadows. The most severe and acute disturbance to nearshore seagrass meadows in the region in recent years has been the periodic mass influxes of sargassum, which are believed to be caused by changes in the Atlantic Ocean due to climate change and regionwide eutrophication. Onshore accumulation of massive quantities of sargassum creates “brown tides” that deplete light and oxygen, and cause mortality of the benthos in the zone of influence (20–100 m offshore) [97]. When the brown tide subsides, algal communities develop in zones previously colonized by seagrasses [97]. As the recurrence period of the sargassum influx is shorter than the recovery time of a well-developed meadow [97], changes in the nearshore zones are likely to be permanent. In addition, the sargassum influx has changed the water quality in all the reef lagoons, even kilometres offshore [97,117], affecting the seagrass meadow in areas beyond the visible brown tides [105].
Amongst the most concerning trend that affects the seagrass meadows throughout the Caribbean, including Mexico, is a gradual decline in the dominant and most robust seagrass Thalassia testudinum (e.g., Van Tussenbroek et al. [108]), due to increasing anthropogenic disturbances (see above), because this is the most important habitat-forming species that cannot be replaced functionally by any other species. Seagrass meadows dominated by faster growing seagrass species that have inferior rooting capacity are more susceptible to removal during tropical storms or hurricanes. Once lost, the meadows will not recover for at least several decades, as the positive feedbacks that maintained them are gone [118]. A good example of the effect of synergistic disturbance is a 5 ha large seagrass meadow at Akumal, that has undergone a community shift towards S. filiforme and Halodule wrightii due to eutrophication [119]. Turtle overgrazing pushed this system towards a tipping point of an alternate state without seagrasses [111], which has not happened to date, due to the unexpected explosion of calcareous algae that protect the turtle grass from overgrazing by the turtles [112]. However, another study of combined eutrophication and overgrazing (by sea urchins) in Barbados revealed the removal of a sparse S. filiforme meadow remaining after a hydrological anomaly, causing the collapse of the ecosystem, including the loss of the beach [108].

3.3.7. Coral Reefs

The main disturbances affecting coral reefs are linked to tourism activities, hurricanes, overfishing, the spread of disease and exotic species, and the increase in seawater temperatures [120,121,122]. Contreras-Silva et al. [121] estimated that the hard coral cover in the Mexican Caribbean in the 1970s was approximately 26%, decreasing to approximately 16% by 2016. Such changes favour the replacement of corals by fast-growing fleshy macroalgae, which leads to the loss of key ecosystem functions and a phase shift from a coral dominated reef assemblage to a macroalgal-dominated ecosystem [121,122,123].
Poor practices by divers and snorkelers have caused physical damage and the resuspension of sediment on reefs, as observed in various reports [109,124,125]. Damage to corals due to the anchoring of small boats visiting the reef has also been reported [36,125]. The occasional grounding of ships on the reef has been the source of another disturbance [125,126]. Additionally, Axis-Arroyo and Mateu [127] noted that ferry traffic can lead to changes in the composition and abundance of seabed species, especially close to ports, where sediment is constantly resuspended due to the manoeuvring of vessels.
Overfishing is a further cause of damage to the reef, due to the decrease in biomass of different species [37,128]. Overfishing of the spiny lobster (Panulirus argus and P. guttatus), queen conch (Aliger = Lobatus = Strombus gigas), grouper, and snapper has practically annihilated their populations [125].
The lionfish is the invasive species posing the greatest danger to the coastal ecosystems of the Mexican Caribbean today. Lionfish (Pterois volitans) and devilfish (Pterois miles), also sometimes called lionfish, were first observed in the Mexican Caribbean in 2009 and since then, have established across the entire region successfully [129,130], despite active efforts to reduce their populations.
Diseases and bleaching (loss of symbiotic algae) have affected most coral species in the Mexican Caribbean [131]. Coral bleaching has been reported [84,132], and the infectious diseases of greatest concern are Aspergillosis [133,134,135], white band disease [84,135], white pox [84,135], white plague [84,135,136], yellow band disease [133,137,138], black band disease [84,135,136], black spots [135,139], necrotic tissue patches [139], and the recently reported stony coral tissue loss disease [123].
Hurricanes are the most damaging climatic disturbance to coral ecosystems. High-intensity hurricanes (category 4 and 5) can detach branches of coral, sea fans, and sponges, overturn coral colonies, and even destroy entire colonies [140]. Up to 60% of the coral cover in the northern Mexican Caribbean has been lost due to high-intensity hurricanes [141,142,143]. They have also reduced the architectural complexity of the reefs, with negative impacts on biodiversity, composition, and functioning of these reefs [144].
The influx of sargassum has caused the mortality of small colonies in nearshore waters and on artificial reefs, such as Gorgonia flabellum, Palythoa caribaeorum, Diploria labyrinthiformis, Dichocoenia stokesii, Porites astreoides, and Pseudodiploria clivosa [97,145], as well as at least 78 animal species (mostly fish) [117]. Cabanillas-Terán et al. [95] found that the massive arrivals of this alga induced changes in food webs, such as reef algal consumption by sea urchins, which may possibly influence the natural dynamics of coral reef ecosystems.

4. Discussion

Coastal zone management is a complex task from both a social and ecological perspective. From a social point of view, management should ideally seek to meet the sustainable development goals proposed by the United Nations 2030 Agenda for Sustainable Development (no poverty, zero hunger, healthy life, qualitative education, gender equality, and decent work), in addition to meeting the specific needs of the human population at the study site. From an ecological perspective, management must be sustainable, which implies that human developments should not cause the depletion of natural resources or place the environment at risk.
The cities and villas development plans on the Mexican Caribbean coast must consider around 45 laws and regulations on urban development and environmental protection [146]. However, many times these laws have been ignored to foster economic activities. For example, tourism promotes the creation of jobs and a positive economic impact on >70% of the GDP in the state of Quintana Roo [20,34], which is why tourism projects continue to be promoted despite the disturbances related to this activity. The conflicts of interest that represent economic benefits on the one hand and ecosystem sustainability on the other hand, represent a great challenge for coastal zone management in many Caribbean areas.
Analysis of disturbances may help to understand the underlying pressures of a system caused by anthropogenic development, thereby providing guidance as to where to set the limits on natural resource use or occupation of the natural environment so as to avoid compromising the integrity of the system in question. Due to the resilience of many ecosystems (see basins of attraction in Figure 1), it is often difficult to detect the critical point at which a possible regime change occurs. The increase in the number of disturbances, as well as the increase in their frequency, duration, and intensity, decreases the stability of the ecosystem, hence increasing the probability of regime change [9]. Therefore, knowledge of the disturbances at a site will enhance our understanding of the pressure that the system at a particular site is subjected to. Since the main objective of sustainable development is to neither put the environment nor humans at risk, the assessment of disturbances at a study site can be key to achieving the balance between economic growth, environmental care, and social well-being.
The systematic study of disturbances could serve as a helpful tool for use in coastal zone management. One of the main advantages of a study of this type is the precision of the diagnosis that can be carried out in relation to the causes of human intervention and the changes in the natural flow of coastal processes [147,148]. Once the sources of disturbance have been identified, different frameworks may be applied to assess the spatial–temporal effectiveness of different responses to disturbances. Such frameworks include DPSIR (Drivers-Pressure-State-Impact-Response) [149]; DAPSI(W)R(M) (Driver-Activity-Pressure-State change-Impacts (on Welfare)-Responses (through Measures) [150]; and DESCR (Drivers-Exchanges-States-Consequences-Responses) [151]. For these frameworks, data associated with anthropogenic disturbances is particularly useful for assessing the impacts or consequences of human activities.
Based on the DESCR framework, drivers are considered anything that can stimulate any form of mass and energy flow, whether it be natural (natural disturbances) or anthropogenic (human-induced disturbances) and of local, regional, or global origin. The effects of these drivers are then reflected in the exchanges of mass or energy flow that modify the environment manifesting either as long-term chronic processes (e.g., gradual nutrient input) or processes that show up episodically (e.g., passage of a hurricane). In this framework, the assessment of the consequences (e.g., social, economic, or in ecosystem services) helps to provide potential responses for adaptive coastal management (e.g., wastewater treatment, restoration of seagrass beds).
For example, a major disturbance in the municipality of Benito Juarez has been the change in land use associated with the creation of the hotel zone in Cancun. The resultant urbanization (mostly streets and buildings) has affected practically 100% of the barrier island (known as the hotel zone) surrounding the Nichupté lagoon system. Hurricanes Gilbert in 1988 and Wilma in 2005 caused “shifts” in the morphodynamic behaviour of the barrier island [75,152,153]. Up until the late 1960s, the barrier island was uninhabited and comprised sand dunes and beaches set among mangroves, lagoons, and rainforest landscape [154]. The small intermittent inlets that were formed during severe storms and healthy dune systems enabled the recirculation of water and sediments between the sea and the lagoon, maintaining the natural balance of the sediments and a dynamic beach-dune system. Given the fact that mass construction, in the form of tourism infrastructure, has been carried out over the last five decades, the barrier island, in morphodynamic terms, now acts as a giant concrete dam [75,151,155]. During intense wave activity and storm tides, the beach undergoes transformation, with sediment moving out from the dune and into the sea. However, in the absence of dunes, when the waves hit the buildings that have been erected directly on the shoreline, the wave energy is no longer dissipated to the same degree. Wave reflection, induced by the coastal infrastructure, increases the intensity of the surf and causes the sediment to move, leaving the littoral cell. Another consequence of the building of infrastructure is a significant reduction in water renewal within the Nichupté lagoon system. The increased retention time has led to the following: (1) chronic eutrophication due to limited water exchange with the Nichupté lagoon (see seagrass systems above), (2) flooding of the barrier island has become more frequent and for longer periods due to lack of drainage caused by the presence of paved surfaces limiting percolation to the subsoil and solid infrastructure preventing efficient surface runoff to the sea and the lagoon, and (3) the loss of beaches and dunes associated with increased sediment transport offshore [75].
Following the passage of Hurricane Gilbert in 1988, inadequate structural remediation measures were carried out in Cancun, leading to a further decline of the system’s resilience, the result of having failed to properly identify anthropogenic disturbances, [156]. After the passage of Hurricane Wilma in 2005, it became clear that the responses had been inadequate in the past and that the socioeconomic consequences of the damage were much more significant. The decision was made to, as a remedial measure, provide artificial beach nourishment to two beaches (importing more than 8 million m3 of sand) [157] and to build a beach protection structure in the northern area of Quintana Roo. However, according to Martell et al. [79], the morphodynamic imbalance of the barrier island of Cancun is an ongoing problem, and future disturbances by hurricanes or storms will critically impact the area and create a critical state again.
In addition to the anthropogenic disturbances of local origin (such as the example above), we must also consider disturbances that occur at a regional level (for example, contamination of the groundwater) or global origin (for example, those associated with climate change). Identifying these disturbances and assessing their outcomes (even qualitatively) can undoubtedly help to define potential response actions. Such actions seek to adaptively modify the responses with the aim of reducing negative impacts and improving the conditions of the systems that will form part of the new Drivers-Exchanges-States cycle.
In the Mexican Caribbean, anthropogenic disturbances have caused significant changes to the main ecosystems of Puerto Morelos that include the following: coral reefs, seagrass meadows in the reef lagoon, beaches, dunes, and mangroves. Here, the mangroves are separated from the sea by the dunes and beach (sand barrier), and at present they are only connected with the sea during storm conditions [151]. In the continental part, the major local disturbance is urbanization [67]. Urbanization of the sand barrier has obstructed the water and sediment recirculation between the mangrove and the sea. Roads crossing the mangrove have modified the water flow within the mangrove wetland, generating stagnation of the water in certain areas and desiccation in others. Wastewater discharge into the aquifer is both a local and regional anthropogenic disturbance that also affects the marine ecosystem, because polluted groundwater is discharged through submarine springs into mangroves and the reef lagoon. In Puerto Morelos, rising water temperature due to global climate change has caused coral bleaching and subsequent coral death [158]. Coral bleaching and diseases have resulted in the loss of structural complexity and a reduction in wave energy dissipation through turbulence and friction, thus wave breaking is drastically reduced [159]. Furthermore, fleshy macroalgae colonize the reef substrate, further modifying the configuration of this ecosystem [123]. The mass influx of sargassum (either a regional or global disturbance depending on its hypothesized causes), has resulted in changes in the physical–chemical parameters of seawater, including temperature, light, pH, and nutrient concentrations, with potential far-reaching consequences for all associated marine ecosystems [97]. Thus, Puerto Morelos is exposed to anthropogenic disturbances of local, regional, and global origin; although the consequences of each of these disturbances could be assessed to a certain degree, the consequences of their interactive impacts, on top of interactions with natural disturbances, are extremely difficult to assess.
Using the PRISMA framework, the disturbances that affect the Mexican Caribbean study site were identified in a systematic manner. However, as the methodology was developed, certain limitations became apparent. For example, it was not possible to determine whether the disturbances referred to in earlier publications are still ongoing or not, or, if the values reported have increased or decreased over time. Moreover, it was not possible to know if the impacts of these disturbances continue, or, if these ecosystems have recovered. In addition, when analysing such a wide area, it is important to pinpoint the location of the disturbances in order to recommend targeted management strategies because not all disturbances occur across the entire study area. The way to use the information produced by PRISMA to the greatest advantage is to clearly identify both the location and the period in which the reported disturbances occurred. On a final note, it is important to highlight that the number of reports does not necessarily reflect the total number of disturbances that have occurred in the ecosystems of the Mexican Caribbean.
In the Mexican Caribbean, the loss of coral cover and the consequent flattening of the coral reef landscape has led to a decrease in wave energy dissipation. As a consequence, more energy is transmitted to the shoreline and there is less oxygenation of the seawater. Similarly, the loss of nearshore seagrass meadows has caused waves to strike the beach with more energy. Increased wave energy and lower seagrass cover has resulted in sediment being transported along the shoreline and lost. The loss of sand and their stability promote further fragmentation of seagrass beds. Waves reflecting off the beach and coastal infrastructure carry large amounts of sediment beyond the littoral cell, causing beach erosion. The transport of fine sediment increases turbidity in the water, affecting many coral reef species and resulting in the replacement of seagrasses by algae. These processes bring about cascading impacts due to the decrease in the populations of key species, such as parrotfish that help to maintain a healthy reef structure and generate sand production. Species that can withstand the new conditions, e.g., calcareous algae or lionfish, occupy the niches vacated by species that have been unable to adapt. Given this scenario, disturbances cause the coastal infrastructure to become more exposed and the low-lying areas of the coastline to become flooded, which, in turn, negatively impacts the dune and mangrove vegetation, driving these systems to a regime shift.

5. Conclusions

Anthropogenic disturbances have caused extreme changes to the ecosystems in the Mexican Caribbean. The main anthropogenic disturbances produced locally include the change in land use, predominantly related to the construction of infrastructure, and the pollution of water bodies linked mainly to wastewater discharge, which generate consequences on a regional scale. In addition to local disturbances, global disturbances, such as increased temperatures and the mass influx of sargassum, have caused significant negative impacts on coastal ecosystems. Natural disturbances such as hurricanes may have caused strong impacts on these disturbed ecosystems.
The use of the PRISMA methodology was valuable for helping to determine the agents that trigger disturbances and their origin. This information helps us determine which disturbances we can and cannot control, based on their causes (e.g., natural and global disturbances), and where other response strategies need to be put in place. In addition, this work shows that effective coastal zone management frameworks can be developed by accurately diagnosing the impacts and consequences of human activities on coastal ecosystems. Understanding how human actions exert change over natural processes is important when considering solutions for restoring natural flows. This is particularly important in places where a change of state has been observed. If the changes to natural processes have been well-understood, strategies may be employed to attack the root problem, taking out the guesswork. It is essential to point out that once the key elements of disturbances have been identified and the altered processes have been well-understood, the main goal should be to put the necessary responses in place to achieve the sustainable management of the coast.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jmse10050644/s1, Table S1: Disturbances reported for the municipalities of Quintana Roo and the Mexican Caribbean.

Author Contributions

Conceptualization, I.G., D.L. and R.S.; methodology, I.G. and J.R.; validation, I.G. and J.R.; formal analysis, I.G., J.R., D.L., R.S., B.v.T. and A.T.B.; investigation, I.G., J.R., D.L., R.S., B.v.T. and A.T.B.; resources, I.G.; data curation, I.G., J.R., D.L., R.S., B.v.T. and A.T.B.; writing—original draft preparation, I.G., D.L. and R.S.; writing—review and editing, I.G., J.R., D.L., R.S., B.v.T. and A.T.B. All authors have read and agreed to the published version of the manuscript.

Funding

The authors are grateful to CONACYT-SENER-Sustentabilidad Energética project “Centro Mexicano de Innovación en Energía del Océano (CEMIE Océano)”: FSE-2014-06-249795 for their financial and technical support.

Data Availability Statement

As this is a review article, the data supporting the results can be found in the respective references in the manuscript.

Acknowledgments

The authors thank CONACYT for the grant awarded to Izchel Gómez and Janner Rodríguez.

Conflicts of Interest

The authors declare that there are no conflicts of interest that may affect third parties in relation to the publication of this article.

References

  1. Silva, R.; Chávez, V.; Bouma, T.J.; Van Tussenbroek, B.I.; Arkema, K.K.; Martínez, M.L.; Oumeraci, H.; Heymans, J.J.; Osorio, A.F.; Mendoza, E.; et al. The Incorporation of Biophysical and Social Components in Coastal Management. Estuaries Coasts 2019, 42, 1695–1708. [Google Scholar] [CrossRef][Green Version]
  2. Newman, E.A. Disturbance Ecology in the Anthropocene. Front. Ecol. Evol. 2019, 7, 147. [Google Scholar] [CrossRef][Green Version]
  3. Walker, L.A.; Willig, M.R. An introduction to terrestrial disturbance. In Ecosystem of the World 16: Ecosystems of Disturbed Ground; Walker, L.A., Ed.; Elsevier: Amsterdam, The Netherlands, 1999. [Google Scholar]
  4. Battisti, C.; Poeta, G.; Fanelli, G. An Introduction to Disturbance Ecology; Springer International Publishing: Cham, Switzerland, 2016; ISBN 9783319324753. [Google Scholar]
  5. White, P.S.; Pickett, S.T.A. Chapter 1—Natural Disturbance and Patch Dynamics: An Introduction. In The Ecology of Natural Disturbance and Patch Dynamics; Pickett, S.T.A., White, P.S.B.T., Eds.; Academic Press: San Diego, CA, USA, 1985; pp. 3–13. ISBN 978-0-08-050495-7. [Google Scholar]
  6. Turner, M.G. Disturbance and landscape dynamics in a changing world. Ecology 2010, 91, 2833–2849. [Google Scholar] [CrossRef] [PubMed][Green Version]
  7. Grimm, N.B.; Pickett, S.T.A.; Hale, R.L.; Cadenasso, M.L. Does the ecological concept of disturbance have utility in urban social–ecological–technological systems? Ecosyst. Health Sustain. 2017, 3, e01255. [Google Scholar] [CrossRef]
  8. Connell, J.H. Diversity in Tropical Rain Forests and Coral Reefs. Science 1978, 199, 1302–1310. [Google Scholar] [CrossRef][Green Version]
  9. Tett, P.; Gowen, R.J.; Painting, S.J.; Elliott, M.; Forster, R.; Mills, D.K.; Bresnan, E.; Capuzzo, E.; Fernandes, T.F.; Foden, J.; et al. Framework for understanding marine ecosystem health. Mar. Ecol. Prog. Ser. 2013, 494, 1–27. [Google Scholar] [CrossRef][Green Version]
  10. Sguotti, C.; Cormon, X. Regime Shifts—A Global Challenge for the Sustainable Use of Our Marine Resources BT—YOUMARES 8—Oceans Across Boundaries: Learning from Each Other; Jungblut, S., Liebich, V., Bode, M., Eds.; Springer International Publishing: Cham, Switzerland, 2018; pp. 155–166. [Google Scholar]
  11. Ratajczak, Z.; Carpenter, S.R.; Ives, A.R.; Kucharik, C.J.; Ramiadantsoa, T.; Stegner, M.A.; Williams, J.W.; Zhang, J.; Turner, M.G. Abrupt Change in Ecological Systems: Inference and Diagnosis. Trends Ecol. Evol. 2018, 33, 513–526. [Google Scholar] [CrossRef]
  12. Walker, B.; Holling, C.S.; Carpenter, S.R.; Kinzig, A. Resilience, adaptability and transformability in social-ecological systems. Ecol. Soc. 2004, 9, 5. [Google Scholar] [CrossRef]
  13. Farina, A. Principles and Methods in Landscape Ecology: Toward a Science of Landscape; Springer: Berlin/Heidelberg, Germany, 2006; ISBN 978-1-4020-3327-8. [Google Scholar]
  14. Peters, D.P.C.; Lugo, A.E.; Chapin, F.S.; Pickett, S.T.A.; Duniway, M.; Rocha, A.V.; Swanson, F.J.; Laney, C.; Jones, J. Cross-system comparisons elucidate disturbance complexities and generalities. Ecosphere 2011, 2, 1–26. [Google Scholar] [CrossRef]
  15. Burton, P.J.; Jentsch, A.; Walker, L.R. The ecology of disturbance interactions. Bioscience 2020, 70, 854–870. [Google Scholar] [CrossRef]
  16. De Groot, R.; Van der Perk, J.; Chiesura, A.; Van Vliet, A. Importance and threat as determining factors for criticality of natural capital. Ecol. Econ. 2003, 44, 187–204. [Google Scholar] [CrossRef]
  17. Mittermeier, R.; Gil, P.; Hoffmann, M.; Pilgrim, J.; Brooks, T.; Mittermeier, C.; Lamoreux, J.; Fonseca, G. Hotspots Revisited. Earth’s Biologically Richest and Most Endangered Terrestrial Ecoregions; Cemex: Monterrey, Mexico, 2004; Volume 392, ISBN 968-6397-77-9. [Google Scholar]
  18. Ellis, E.A.; Hernández-Gómez, I.U.; Romero-Montero, J.A. Los procesos y causas del cambio en la cobertura forestal de la Península Yucatán, México. Ecosistemas 2017, 26, 101–111. [Google Scholar] [CrossRef]
  19. Tittensor, D.P.; Mora, C.; Jetz, W.; Lotze, H.K.; Ricard, D.; Berghe, E.V.; Worm, B. Global patterns and predictors of marine biodiversity across taxa. Nature 2010, 466, 1098–1101. [Google Scholar] [CrossRef]
  20. Banaszak, A.T. Anthropogenic Pollution of Aquatic Ecosystems. In Contamination of Coral Reefs in the Mexican Caribbean; Häder, D., Helbling, E.W., Villafañe, V.E., Eds.; Springer International Publishing: Cham, Switzerland, 2021; pp. 113–129. ISBN 9783030756024. [Google Scholar]
  21. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. Int. J. Surg. 2021, 88, 105906. [Google Scholar] [CrossRef]
  22. Tello, H.; Castellanos, E. Caracteristicas geograficas. In Riqueza Biológica de Quintana Roo. Un Análisis para su Conservación, Tomo I.; Pozo, C., Armijo Canto, N., Calmé, S., Eds.; El Colegio de la Frontera Sur (ECOSUR), Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (Conabio), Gobierno del Estado de Quintana Roo y Programa de Pequeñas Donaciones (PPD): Mexico City, Mexico, 2011; p. 83. [Google Scholar]
  23. Beddows, P.A. Where does the sewage go? The karst groundwater system of municipalidad Solidaridad, Quintana Roo. AMCS Act. Newsl. 2002, 25, 47–52. [Google Scholar]
  24. Bauer-Gottwein, P.; Gondwe, B.R.N.; Charvet, G.; Marín, L.E.; Rebolledo-Vieyra, M.; Merediz-Alonso, G. Review: The Yucatán Peninsula karst aquifer, Mexico. Hydrogeol. J. 2011, 19, 507–524. [Google Scholar] [CrossRef]
  25. Deng, Y.; Young, C.; Fu, X.; Song, J.; Peng, Z.R. The integrated impacts of human activities and rising sea level on the saltwater intrusion in the east coast of the Yucatan Peninsula, Mexico. Nat. Hazards 2017, 85, 1063–1088. [Google Scholar] [CrossRef]
  26. Metcalfe, C.D.; Beddows, P.A.; Bouchot, G.G.; Metcalfe, T.L.; Li, H.; Van Lavieren, H. Contaminants in the coastal karst aquifer system along the Caribbean coast of the Yucatan Peninsula, Mexico. Environ. Pollut. 2011, 159, 991–997. [Google Scholar] [CrossRef]
  27. Pérez-Moreno, J.L.; Iliffe, T.M.; Bracken-Grissom, H.D. Life in the Underworld: Anchialine cave biology in the era of speleogenomics. Int. J. Speleol. 2016, 45, 149–170. [Google Scholar] [CrossRef][Green Version]
  28. Beddows, P.A.; Smart, P.L.; Whitaker, F.F.; Smith, S.L. Decoupled fresh-saline groundwater circulation of a coastal carbonate aquifer: Spatial patterns of temperature and specific electrical conductivity. J. Hydrol. 2007, 346, 18–32. [Google Scholar] [CrossRef]
  29. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO) Portal de Información Geográfica. Available online: http://www.conabio.gob.mx/informacion/gis/ (accessed on 26 March 2020).
  30. United Nations Environment Programme-Environment World Conservation Monitoring Centre (UNEP-WCMC) Ocean Data Viewer. Available online: https://data.unep-wcmc.org/ (accessed on 29 March 2020).
  31. Ramírez-Barajas, P.; Islebe, G.A.; Torrescano-Valle, N. Perturbación post-huracán Dean en el hábitat y la abundancia relativa de vertebrados mayores de la Selva Maya, Quintana Roo, México. Rev. Mex. Biodivers. 2012, 83, 1194–1207. [Google Scholar] [CrossRef][Green Version]
  32. Ardisson, P.-L.; May-Kú, M.A.; Herrera-Dorantes, M.T.; Arellano-Guillermo, A. The Mesoamerican Barrier Reef System-Mexico: Considerations for its designation as a Particularly Sensitive Sea Area. Hidrobiologica 2011, 21, 261–280. [Google Scholar]
  33. Beltrán-Torres, A. Ecosistemas marinos. In Riqueza Biológica de Quintana Roo. Un Análisis para su Conservación, Tomo I.; Pozo, C., Armijo Canto, N., Calmé, S., Eds.; El Colegio de la Frontera Sur (ECOSUR), Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (Conabio), Gobierno del Estado de Quintana Roo y Programa de Pequeñas Donaciones (PPD): Mexico City, Mexico, 2011; p. 83. [Google Scholar]
  34. Sánchez-Gil, P.; Yáñez-Arancibia, A.; Ramírez-Gordillo, J.; Day, J.W.; Templet, P.H. Some socio-economic indicators in the Mexican states of the Gulf of Mexico. Ocean Coast. Manag. 2004, 47, 581–596. [Google Scholar] [CrossRef]
  35. Babinger, F. Tourism facing the challenge of recurring natural hazards: A view from Cancún. Investig. Geogr. 2012, 78, 75–88. [Google Scholar] [CrossRef]
  36. Solís-Weiss, V.; Alejandro, G.B.; Martínez, J.M. Environmental evaluation of Cozumel Island Mexico. In Proceedings of the 8th International Conference on the Mediterranean Coastal Environment, Alexandria, Egypt, 13–17 November 2007; Volume 2, pp. 775–786. [Google Scholar]
  37. Figueroa-Zavala, B.; Correa-Sandoval, J.; Ruiz-Zárate, M.Á.; Weissenberger, H.; González-Solís, D. Environmental and socioeconomic assessment of a poorly known coastal section in the southern Mexican Caribbean. Ocean Coast. Manag. 2015, 110, 25–37. [Google Scholar] [CrossRef]
  38. Abraham, A.G.; Schmook, B.; Calmé, S. Distribución espacio-temporal de las actividades extractivas en los bosques del ejido Caoba, Quintana Roo. Investig. Geogr. 2007, 62, 69–86. [Google Scholar] [CrossRef]
  39. Ellis, E.A.; Navarro Martínez, A.; García Ortega, M.; Hernández Gómez, I.U.; Chacón Castillo, D. Forest cover dynamics in the Selva Maya of Central and Southern Quintana Roo, Mexico: Deforestation or degradation? J. Land Use Sci. 2020, 15, 25–51. [Google Scholar] [CrossRef]
  40. Ellis, E.A.; Romero Montero, J.A.; Hernández Gómez, I.U. Deforestation processes in the state of quintana roo, mexico: The role of land use and community forestry. Trop. Conserv. Sci. 2017, 10, 1940082917697259. [Google Scholar] [CrossRef][Green Version]
  41. Rada, J.M.; Iturbe, J.A.; Vivar, S.I.; Irabien, L.M.; Manrique, C.; Dzul, F.; Euán, A. Cambios de cobertura y uso del suelo (1979–2000) en dos comunidades rurales en el noroeste de Quintana Roo. Investig. Geogr. 2007, 62, 104–124. [Google Scholar]
  42. Rodríguez-Trejo, D.A.; Tchikoué, H.; Cíntora-González, C.; Contreras-Aguado, R.; De la Rosa-Vázquez, A. Modelaje del peligro de incendio forestal en las zonas afectadas por el huracán Dean. Agrociencia 2011, 45, 593–608. [Google Scholar]
  43. Andrade-Herrera, M.; Escalona-Segura, G.; González-Jáuregui, M.; Reyna-Hurtado, R.A.; Vargas-Contreras, J.A.; Rendón-von Osten, J. Presence of Pesticides and Toxicity Assessment of Agricultural Soils in the Quintana Roo Mayan Zone, Mexico Using Biomarkers in Earthworms (Eisenia fetida). Water. Air. Soil Pollut. 2019, 230, 59. [Google Scholar] [CrossRef]
  44. González-Gallina, A.; Hidalgo-Mihart, M.G.; Castelazo-Calva, V. Conservation implications for jaguars and other neotropical mammals using highway underpasses. PLoS ONE 2018, 13, e0206614. [Google Scholar] [CrossRef] [PubMed][Green Version]
  45. Mazzotti, F.J.; Fling, H.E.; Merediz, G.; Lazcano, M.; Lasch, C. Conceptual ecological model of the Sian Ka’an Biosphere Reserve, Quintana Roo, Mexico. Wetlands 2005, 25, 980–997. [Google Scholar] [CrossRef]
  46. Cairns, C.E.; Villanueva-Gutiérrez, R.; Koptur, S.; Bray, D.B. Bee Populations, Forest Disturbance, and Africanization in Mexico. Biotropica 2005, 37, 686–692. [Google Scholar] [CrossRef]
  47. Martínez-Morales, M.A.; Cuarón, A.D. Boa constrictor, an introduced predator threatening the endemic fauna on Cozumel Island, Mexico. Biodivers. Conserv. 1999, 8, 957–963. [Google Scholar] [CrossRef]
  48. Romero-Nájera, I.; Cuarón, A.D.; González-Baca, C. Distribution, abundance, and habitat use of introduced Boa constrictor threatening the native biota of Cozumel Island, Mexico. Biodivers. Conserv. 2007, 16, 1183–1195. [Google Scholar] [CrossRef]
  49. Suárez-Atilano, M.; Cuarón, A.D.; Vázquez-Domínguez, E. Deciphering Geographical Affinity and Reconstructing Invasion Scenarios of Boa imperator on the Caribbean Island of Cozumel. Copeia 2019, 107, 606–621. [Google Scholar] [CrossRef]
  50. Cedeño-Vázquez, J.R.; González-Vázquez, J.; Martínez-Arce, A.; Canseco-Márquez, L. First record of the invasive greenhouse frog (Eleutherodactylus planirostris) in the Mexican Caribbean. Rev. Mex. Biodivers. 2014, 85, 650–653. [Google Scholar] [CrossRef][Green Version]
  51. Machkour-M’Rabet, S.; Vilchis-Nestor, C.A.; Barriga-Sosa, I.D.L.A.; Legal, L.; Hénaut, Y. A molecular approach to understand the riddle of the invasive success of the tarantula, Brachypelma vagans, on Cozumel Island, Mexico. Biochem. Syst. Ecol. 2017, 70, 260–267. [Google Scholar] [CrossRef]
  52. Ortega-Morales, A.I.; Bond, G.; Méndez-López, R.; Garza-Hernández, J.A.; Hernández-Triana, L.M.; Casas-Martínez, M. First record of invasive mosquito aedes albopictus in tabasco and yucatan, MEXICO. J. Am. Mosq. Control Assoc. 2018, 34, 120–123. [Google Scholar] [CrossRef][Green Version]
  53. Degante-González, A.P.; Tepatlán-Vargas, R.; Ramírez-Utrera, A.L.; Mora-Heredia, E.; Villegas-Patraca, R. Record of the tricolored munia (Lonchura malacca) in the Isthmus of Tehuantepec, Oaxaca, Mexico. Rev. Mex. Biodivers. 2018, 89, 582–586. [Google Scholar] [CrossRef]
  54. Ramírez-Albores, J.E.; Pérez-Suárez, M. Tropical forest remnants as shelters of avian diversity within a tourism development matrix in yucatan Peninsula, Mexico. Rev. Biol. Trop. 2018, 66, 799–813. [Google Scholar] [CrossRef]
  55. Recuero, E. The invasive species Cylindrodesmus hirsutus Pocock (Diplopoda: Polydesmida: Haplodesmidae) spreads to the northern Caribbean, with a compilation of published localities. Int. J. Trop. Insect Sci. 2018, 38, 299–302. [Google Scholar] [CrossRef]
  56. Cid-Mora, O.; Vásquez-Cruz, V. Nuevo registro en la dieta de la bejuquillo parda Oxybelis aeneus (Serpentes: Colubridae). Rev. Latinoam. Herpetol. 2020, 3, 98–100. [Google Scholar]
  57. Schultz, G.P. Vascular flora of the El Edén Ecological Reserve, Quintana Roo, Mexico. J. Torrey Bot. Soc. 2005, 132, 311–322. [Google Scholar] [CrossRef]
  58. Horwich, R.H. Effective solutions for howler conservation. Int. J. Primatol. 1998, 19, 579–598. [Google Scholar] [CrossRef]
  59. National Oceanic and Atmospheric Administration (NOAA) Historical Hurricane Tracks. Available online: https://coast.noaa.gov/hurricanes/#map=4/32/-80 (accessed on 1 April 2021).
  60. Clifton, D. Yucatan after the wind: Human and environmental impact of hurricane Gilbert in the central and Eastern Yucatan Peninsula. GeoJournal 1991, 23, 337–345. [Google Scholar] [CrossRef]
  61. Gutiérrez-Granados, G.; Juárez, V.; Alcalá, R.E. Natural and human disturbances affect natural regeneration of Swietenia macrophylla: Implications for rainforest management. For. Ecol. Manag. 2011, 262, 161–169. [Google Scholar] [CrossRef]
  62. Garza-López, M.; Ortega-Rodríguez, J.M.; Zamudio-Sánchez, F.J.; López-Toledo, J.F.; Domínguez-Álvarez, F.A.; Sáenz-Romero, C. Calakmul como refugio de Swietenia macrophylla King ante el cambio climático. Bot. Sci. 2016, 94, 76–87. [Google Scholar] [CrossRef][Green Version]
  63. Heénaut, Y.; Corbara, B.; Peélozuelo, L.; Azeémar, F.; Ceéreéghino, R.; Herault, B.; Dejean, A. A tank bromeliad favors spider presence in a neotropical inundated forest. PLoS ONE 2014, 9, e114592. [Google Scholar] [CrossRef][Green Version]
  64. León-Borges, J.A.; Lizardi-Jiménez, M.A. Hydrocarbon pollution in underwater sinkholes of the Mexican Caribbean caused by tourism and asphalt: Historical data series and cluster analysis. Tour. Manag. 2017, 63, 179–186. [Google Scholar] [CrossRef]
  65. Kambesis, P.N.; Coke, J.G. The sac actun system, Quintana Roo, Mexico. Bol. Geol. y Min. 2016, 127, 177–192. [Google Scholar]
  66. Tun-Canto, G.E.; Álvarez-Legorreta, T.; Zapata-Buenfil, G.; Sosa-Cordero, E. Metales pesados en suelos y sedimentos de la zona cañera del sur de Quintana Roo, México. Rev. Mex. Ciencias Geol. 2017, 34, 157–169. [Google Scholar] [CrossRef][Green Version]
  67. Hernández-Terrones, L.; Rebolledo-Vieyra, M.; Merino-Ibarra, M.; Soto, M.; Le-Cossec, A.; Monroy-Ríos, E. Groundwater pollution in a karstic region (NE Yucatan): Baseline nutrient content and flux to coastal ecosystems. Water. Air. Soil Pollut. 2011, 218, 517–528. [Google Scholar] [CrossRef]
  68. Leal-Bautista, R.M.; Hernández-Zárate, G.; Jaime, M.N.A.; Cuevas, R.G.; Oliman, G.V. Pathogens and pharmaceuticals pollutants as indicators of contamination at the northeasthern aquifer of quintana roo. Trop. Subtrop. Agroecosyst. 2011, 13, 211–219. [Google Scholar]
  69. Chávez, V.; Uribe-Martínez, A.; Cuevas, E.; Rodríguez-Martínez, R.E.; Van Tussenbroek, B.I.; Francisco, V.; Estévez, M.; Celis, L.B.; Monroy-Velázquez, L.V.; Leal-Bautista, R.; et al. Massive influx of pelagic sargassum spp. On the coasts of the mexican caribbean 2014–2020: Challenges and opportunities. Water 2020, 12, 2908. [Google Scholar] [CrossRef]
  70. Casas-Beltran, D.A.; Hernández-Pedraza, M.; Alvarado-Flores, J. Estimation of the discharge of sunscreens in aquatic environments of the Mexican Caribbean. Environments 2020, 7, 15. [Google Scholar] [CrossRef][Green Version]
  71. Parra, S.M.; Valle-Levinson, A.; Mariño-Tapia, I.; Enriquez, C.; Candela, J.; Sheinbaum, J. Seasonal variability of saltwater intrusion at a point-source submarine groundwater discharge. Limnol. Oceanogr. 2016, 61, 1245–1258. [Google Scholar] [CrossRef]
  72. Hirales-Cota, M. Drivers of mangrove deforestation in Mahahual-Xcalak, Quintana Roo, southeast Mexico. Ciencias Mar. 2010, 36, 147–159. [Google Scholar] [CrossRef]
  73. Pedrozo-Acuña, A.; Damania, R.; Laverde-Barajas, M.A.; Mira-Salama, D. Assessing the consequences of sea-level rise in the coastal zone of Quintana Roo, México: The costs of inaction. J. Coast. Conserv. 2015, 19, 227–240. [Google Scholar] [CrossRef]
  74. Almeida, L.R.; Silva, R.; Martínez, M.L. The relationships between environmental conditions and parallel ecosystems on the coastal dunes of the Mexican Caribbean. Geomorphology 2021, 397, 108006. [Google Scholar] [CrossRef]
  75. Casarin, R.S.; Martinez, G.R.; Mariño-Tapia, I.; Vanegas, G.P.; Baldwin, E.M.; Mancera, E.E. Manmade Vulnerability of the Cancun Beach System: The Case of Hurricane Wilma. Clean-Soil Air Water 2012, 40, 911–919. [Google Scholar] [CrossRef]
  76. Martell-Dubois, R.; Mendoza-Baldwin, E.; Mariño-Tapia, I.; Silva-Casarín, R.; Escalante-Mancera, E. Impactos de corto plazo del huracán Dean sobre la morfología de la playa de Cancún, México. Tecnol. Cienc. Agua 2012, 3, 89–111. [Google Scholar]
  77. Ruiz-Martínez, G.; Silva-Casarín, R.; Posada-Vanegas, G. Morphodynamic comparison of the Northeast shoreline of Quintana Roo, Mexico. Tecnol. Cienc. Agua 2013, 4, 47–65. [Google Scholar]
  78. Odériz, I.; Mendoza, E.; Leo, C.; Santoyo, G.; Silva, R.; Martínez, R.; Grey, E.; López, R. An alternative solution to erosion problems at Punta Bete-Punta Maroma, Quintana Roo, Mexico: Conciliating tourism and nature. J. Coast. Res. 2014, 71, 75–85. [Google Scholar] [CrossRef]
  79. Martell, R.; Mendoza, E.; Mariño-Tapia, I.; Odériz, I.; Silva, R. How effective were the beach nourishments at Cancun? J. Mar. Sci. Eng. 2020, 8, 388. [Google Scholar] [CrossRef]
  80. Santos, K.C.; Livesey, M.; Fish, M.; Lorences, A.C. Climate change implications for the nest site selection process and subsequent hatching success of a green turtle population. Mitig. Adapt. Strateg. Glob. Chang. 2017, 22, 121–135. [Google Scholar] [CrossRef]
  81. Ocaña, F.A.; De Jesús-Navarrete, A.; De Jesús-Carrillo, R.M.; Oliva-Rivera, J.J. Efectos del disturbio humano sobre la dinámica poblacional de Ocypode quadrata (Decapoda: Ocypodidae) en playas del Caribe Mexicano. Rev. Biol. Trop. 2016, 64, 1625–1641. [Google Scholar] [CrossRef][Green Version]
  82. Oliver de la Esperanza, A.; Arenas Martínez, A.; Tzeek Tuz, M.; Pérez-Collazos, E. Are anthropogenic factors affecting nesting habitat of sea turtles? The case of Kanzul beach, Riviera Maya-Tulum (Mexico). J. Coast. Conserv. 2017, 21, 85–93. [Google Scholar] [CrossRef][Green Version]
  83. Null, K.A.; Knee, K.L.; Crook, E.D.; De Sieyes, N.R.; Rebolledo-Vieyra, M.; Hernández-Terrones, L.; Paytan, A. Composition and fluxes of submarine groundwater along the Caribbean coast of the Yucatan Peninsula. Cont. Shelf Res. 2014, 77, 38–50. [Google Scholar] [CrossRef][Green Version]
  84. Rodríguez-Martínez, R.E.; Ruíz-Rentería, F.; Van Tussenbroek, B.; Barba-Santos, G.; Escalante-Mancera, E.; Jordán-Garza, G.; Jordán-Dahlgren, E. Environmental state and tendencies of the Puerto Morelos CARICOMP site, Mexico. Rev. Biol. Trop. 2010, 58, 23–43. [Google Scholar] [CrossRef]
  85. Valdes-Lozano, D.S.; Chumacero, M.; Real, E. Sediment oxygen consumption in a developed coastal lagoon of the Mexican Caribbean. Indian J. Mar. Sci. 2006, 35, 227–234. [Google Scholar]
  86. Reyes, E.; Merino, M. Diel dissolved oxygen dynamics and eutrophication in a shallow, well-mixed tropical lagoon (Cancun, Mexico). Estuaries 1991, 14, 372–381. [Google Scholar] [CrossRef]
  87. Baker, D.M.; Rodríguez-Martínez, R.E.; Fogel, M.L. Tourism’s nitrogen footprint on a Mesoamerican coral reef. Coral Reefs 2013, 32, 691–699. [Google Scholar] [CrossRef]
  88. Livingston, R.; McGlynn, S.E.; Niu, X. Factors controlling seagrass growth in a gulf coastal system: Water and sediment quality and light. Aquat. Bot. 1998, 60, 135–159. [Google Scholar] [CrossRef]
  89. Romero-Jarero, J.M.; Del Pilar Negrete-Redondo, M. Presencia de bacterias Gram positivas en músculo de pescado con importancia comercial en la zona del Caribe mexicano. Rev. Mex. Biodivers. 2011, 82, 599–606. [Google Scholar] [CrossRef]
  90. Ortiz-Hernández, M.C.; Sáenz-Morales, R. Effects of organic material and distribution of fecal coliforms in Chetumal Bay, Quintana Roo, Mexico. Environ. Monit. Assess. 1999, 55, 423–434. [Google Scholar] [CrossRef]
  91. Hernández-Terrones, L.M.; Null, K.A.; Ortega-Camacho, D.; Paytan, A. Water quality assessment in the Mexican Caribbean: Impacts on the coastal ecosystem. Cont. Shelf Res. 2015, 102, 62–72. [Google Scholar] [CrossRef]
  92. Sánchez, A.; Álvarez-Legorreta, T.; Sáenz-Morales, R.; Ortiz-Hernández, M.C.; López-Ortiz, B.E.; Aguíñiga, S. Distribution of textural parameters of surficial sediments in the Bay of Chetumal: Implications for the inference of transport. Rev. Mex. Ciencias Geol. 2008, 25, 523–532. [Google Scholar]
  93. Romero-Calderón, A.G.; Morales-Vela, B.; Rosíles-Martínez, R.; Olivera-Gómez, L.D.; Delgado-Estrella, A. Metals in Bone Tissue of Antillean Manatees from the Gulf of Mexico and Chetumal Bay, Mexico. Bull. Environ. Contam. Toxicol. 2016, 96, 9–14. [Google Scholar] [CrossRef]
  94. García-Ríos, V.; Gold-Bouchot, G. Trace metals in sediments from Bahia de Chetumal, Mexico. Bull. Environ. Contam. Toxicol. 2003, 70, 1228–1234. [Google Scholar] [CrossRef]
  95. Cabanillas-Teran, N.; Hernandez-Arana, H.A.; Ruiz-Zarate, M.A.; Vega-Zepeda, A.; Sanchez-Gonzalez, A. Sargassum blooms in the Caribbean alter the trophic structure of the sea urchin Diadema antillarum. PeerJ 2019, 7, e7589. [Google Scholar] [CrossRef][Green Version]
  96. Rodríguez-Martínez, R.E.; Roy, P.D.; Torrescano-Valle, N.; Cabanillas-Terán, N.; Carrillo-Domínguez, S.; Collado-Vides, L.; García-Sánchez, M.; Van Tussenbroek, B.I. Element concentrations in pelagic Sargassum along the Mexican Caribbean coast in 2018-2019. PeerJ 2020, 8, e8667. [Google Scholar] [CrossRef][Green Version]
  97. Van Tussenbroek, B.; Hernández-Arana, H.; Rodríguez-Martínez, R.; Espinoza-Avalos, J.; Canizales-Flores, H.; González-Godoy, C.; Barba-Santos, M.G.; Vega-Zepeda, A.; Collado-Vides, L. Severe impacts of brown tides caused by Sargassum spp. on near-shore Caribbean seagrass communities. Mar. Pollut. Bull. 2017, 122, 272–281. [Google Scholar] [CrossRef]
  98. Sánchez, A.; Ortiz-Hernández, M.C.; Talavera-Sáenz, A.; Aguíñiga-García, S. Stable nitrogen isotopes in the turtle grass Thalassia testudinum from the Mexican Caribbean: Implications of anthropogenic development. Estuar. Coast. Shelf Sci. 2013, 135, 86–93. [Google Scholar] [CrossRef]
  99. Cuellar-Martinez, T.; Ruiz-Fernández, A.C.; Sanchez-Cabeza, J.A.; Pérez-Bernal, L.; López-Mendoza, P.G.; Carnero-Bravo, V.; Agraz-Hernández, C.M.; Van Tussenbroek, B.I.; Sandoval-Gil, J.; Cardoso-Mohedano, J.G.; et al. Temporal records of organic carbon stocks and burial rates in Mexican blue carbon coastal ecosystems throughout the Anthropocene. Glob. Planet. Change 2020, 192, 103215. [Google Scholar] [CrossRef]
  100. Pérez-Gómez, J.A.; García-Mendoza, E.; Olivos-Ortiz, A.; Paytan, A.; Rebolledo-Vieyra, M.; Delgado-Pech, B.; Almazán-Becerril, A. Indicators of nutrient enrichment in coastal ecosystems of the northern Mexican Caribbean. Ecol. Indic. 2020, 118, 106756. [Google Scholar] [CrossRef]
  101. Carruthers, T.J.B.; Van Tussenbroek, B.I.; Dennison, W.C. Influence of submarine springs and wastewater on nutrient dynamics of Caribbean seagrass meadows. Estuar. Coast. Shelf Sci. 2005, 64, 191–199. [Google Scholar] [CrossRef]
  102. Van Tussenbroek, B.I.; Hermus, K.; Tahey, T. Biomass and growth of the turtle grass Thalassia testudinum (Banks ex König) in a shallow tropical lagoon system, in relation to tourist development. Caribb. J. Sci. 1996, 32, 357–364. [Google Scholar]
  103. Whelan, T.; Van Tussenbroek, B.I.; Barba Santos, M.G. Changes in trace metals in Thalassia testudinum after hurricane impacts. Mar. Pollut. Bull. 2011, 62, 2797–2802. [Google Scholar] [CrossRef]
  104. Camacho-Cruz, K.A.; Ortiz-Hernández, M.C.; Sánchez, A.; Carrillo, L.; De Jesús Navarrete, A. Water quality in the eastern karst region of the Yucatan Peninsula: Nutrients and stable nitrogen isotopes in turtle grass, Thalassia testudinum. Environ. Sci. Pollut. Res. 2020, 27, 15967–15983. [Google Scholar] [CrossRef] [PubMed]
  105. Hedley, J.D.; Velázquez-Ochoa, R.; Enríquez, S. Seagrass Depth Distribution Mirrors Coastal Development in the Mexican Caribbean—An Automated Analysis of 800 Satellite Images. Front. Mar. Sci. 2021, 8, 733169. [Google Scholar] [CrossRef]
  106. Cortés, J.; Oxenford, H.A.; Van Tussenbroek, B.I.; Jordán-Dahlgren, E.; Cróquer, A.; Bastidas, C.; Ogden, J.C. The CARICOMP network of caribbean marine laboratories (1985-2007): History, key findings, and lessons learned. Front. Mar. Sci. 2019, 5, 519. [Google Scholar] [CrossRef]
  107. Van Tussenbroek, B.I. Dynamics of seagrasses and associated algae in coral reef lagoons. Hidrobiologica 2011, 21, 293–310. [Google Scholar]
  108. Van Tussenbroek, B.I.; Cortés, J.; Collin, R.; Fonseca, A.C.; Gayle, P.M.H.; Guzmán, H.M.; Jácome, G.E.; Juman, R.; Koltes, K.H.; Oxenford, H.A.; et al. Caribbean-wide, long-term study of seagrass beds reveals local variations, shifts in community structure and occasional collapse. PLoS ONE 2014, 9, e90600. [Google Scholar] [CrossRef][Green Version]
  109. Rioja-Nieto, R.; Sheppard, C. Effects of management strategies on the landscape ecology of a Marine Protected Area. Ocean Coast. Manag. 2008, 51, 397–404. [Google Scholar] [CrossRef]
  110. Herrera-Silveira, J.A.; Cebrian, J.; Hauxwell, J.; Ramirez-Ramirez, J.; Ralph, P. Evidence of negative impacts of ecological tourism on turtlegrass (Thalassia testudinum) beds in a marine protected area of the Mexican Caribbean. Aquat. Ecol. 2010, 44, 23–31. [Google Scholar] [CrossRef]
  111. Molina-Hernández, A.; Van Tussenbroek, B. Patch dynamics and species shifts in seagrass communities under moderate and high grazing pressure by green sea turtles. Mar. Ecol. Prog. Ser. 2014, 517, 143–157. [Google Scholar] [CrossRef]
  112. Leemans, L.; Martínez, I.; Van der Heide, T.; Van Katwijk, M.M.; Van Tussenbroek, B.I. A Mutualism Between Unattached Coralline Algae and Seagrasses Prevents Overgrazing by Sea Turtles. Ecosystems 2020, 23, 1631–1642. [Google Scholar] [CrossRef][Green Version]
  113. Marbà, N.; Gallegos, M.E.; Merino, M.; Duarte, C.M. Vertical growth of Thalassia testudinum: Seasonal and interannual variability. Aquat. Bot. 1994, 47, 1–11. [Google Scholar] [CrossRef]
  114. Cruz-Palacios, V.; Van Tussenbroek, B.I. Simulation of hurricane-like disturbances on a Caribbean seagrass bed. J. Exp. Mar. Bio. Ecol. 2005, 324, 44–60. [Google Scholar] [CrossRef]
  115. Van Tussenbroek, B.I.; Barba Santos, M.G.; Van Dijk, J.K.; Sanabria Alcaraz, S.N.M.; Téllez Calderón, M.L. Selective elimination of rooted plants from a tropical seagrass bed in a back-reef lagoon: A hypothesis tested by Hurricane Wilma (2005). J. Coast. Res. 2008, 24, 278–281. [Google Scholar] [CrossRef]
  116. Van Tussenbroek, B.I.; Guadalupe Barba Santos, M.; Van Dijk, J.K. Unusual synchronous spawning by green algae (Bryopsidales), after the passage of Hurricane Wilma (2005). Bot. Mar. 2006, 49, 270–271. [Google Scholar] [CrossRef][Green Version]
  117. Rodríguez-Martínez, R.E.; Medina-Valmaseda, A.; Blanchon, P.; Monroy-Velázquez, L.; Almazán-Becerril, A.; Delgado-Pech, B.; Vásquez-Yeomans, L.; Francisco, V.; García-Rivas, M. Faunal mortality associated with massive beaching and decomposition of pelagic Sargassum. Mar. Pollut. Bull. 2019, 146, 201–205. [Google Scholar] [CrossRef]
  118. Maxwell, P.S.; Eklöf, J.S.; Van Katwijk, M.M.; O’Brien, K.R.; De la Torre-Castro, M.; Boström, C.; Bouma, T.J.; Krause-Jensen, D.; Unsworth, R.K.F.; Van Tussenbroek, B.I.; et al. The fundamental role of ecological feedback mechanisms for the adaptive management of seagrass ecosystems—A review. Biol. Rev. 2017, 92, 1521–1538. [Google Scholar] [CrossRef][Green Version]
  119. Mutchler, T.; Dunton, K.H.; Townsend-Small, A.; Fredriksen, S.; Rasser, M.K. Isotopic and elemental indicators of nutrient sources and status of coastal habitats in the Caribbean Sea, Yucatan Peninsula, Mexico. Estuar. Coast. Shelf Sci. 2007, 74, 449–457. [Google Scholar] [CrossRef]
  120. Estrada-Saldívar, N.; Jordán-Dalhgren, E.; Rodríguez-Martínez, R.E.; Perry, C.; Alvarez-Filip, L. Functional consequences of the long-term decline of reef-building corals in the Caribbean: Evidence of across-reef functional convergence. R. Soc. Open Sci. 2019, 6, 190298. [Google Scholar] [CrossRef][Green Version]
  121. Contreras-Silva, A.I.; Tilstra, A.; Migani, V.; Thiel, A.; Pérez-Cervantes, E.; Estrada-Saldívar, N.; Elias-Ilosvay, X.; Mott, C.; Alvarez-Filip, L.; Wild, C. A meta-analysis to assess long-term spatiotemporal changes of benthic coral and macroalgae cover in the Mexican Caribbean. Sci. Rep. 2020, 10, 8897. [Google Scholar] [CrossRef]
  122. Rioja-Nieto, R.; Álvarez-Filip, L. Coral reef systems of the Mexican Caribbean: Status, recent trends and conservation. Mar. Pollut. Bull. 2019, 140, 616–625. [Google Scholar] [CrossRef]
  123. Alvarez-Filip, L.; Estrada-Saldívar, N.; Pérez-Cervantes, E.; Molina-Hernández, A.; González-Barrios, F.J. A rapid spread of the stony coral tissue loss disease outbreak in the Mexican Caribbean. PeerJ 2019, 7, e8069. [Google Scholar] [CrossRef][Green Version]
  124. Gil, M.A.; Renfro, B.; Figueroa-Zavala, B.; Penié, I.; Dunton, K.H. Rapid tourism growth and declining coral reefs in Akumal, Mexico. Mar. Biol. 2015, 162, 2225–2233. [Google Scholar] [CrossRef]
  125. Jordan-Dahlgren, E.; Rodriguez-Martinez, R.E. The Atlantic coral reefs of Mexico. In Latin American Coral Reefs; Elsevier: Amsterdam, The Netherlands, 2003; pp. 131–158. ISBN 9780444513885. [Google Scholar]
  126. Ardisson, P.L.; May-Kú, M.A.; Herrera-Dorantes, M.T.; Arellano-Guillermo, A. El Sistema Arrecifal Mesoamericano-México: Consideraciones para su designación como Zona Marítima Especialmente Sensible. Hidrobiologica 2011, 21, 261–280. [Google Scholar]
  127. Axis-Arroyo, J.; Mateu, J. Geostatistical methods for the evaluation of anthropogenic impact in marine bottom. Adv. Ecol. Sci. 2001, 10, 493–499. [Google Scholar]
  128. Arias-González, J.E. Trophic models of protected and unprotected coral reef ecosystems in the South of the Mexican Caribbean. J. Fish Biol. 1998, 53, 236–255. [Google Scholar] [CrossRef]
  129. Rojas, D.C.; Schmitter-Soto, J.J.; Aguilar-Perera, A.; Aguilar Betancourt, C.M.; Ruiz-Zárate, M.; Sansón, G.G.; Chevalier Monteagudo, P.P.; Rodríguez, A.G.; Pavón, R.H.; Valderrama, S.P.; et al. Diversidad de las comunidades de peces en dos áreas marinas protegidas del Caribe y su relación con el pez león. Rev. Biol. Trop. 2018, 66, 189–203. [Google Scholar] [CrossRef][Green Version]
  130. Sabido-Itzá, M.M.; García-Rivas, M.D.C. Record of abundance, spatial distribution and gregarious behavior of invasive lionfish pterois spp. (scorpaeniformes: Scorpaenidae) in coral reefs of banco chinchorro biosphere reserve, Southeastern Mexico. Lat. Am. J. Aquat. Res. 2019, 47, 349–355. [Google Scholar] [CrossRef][Green Version]
  131. Weil, E. Coral Reef Diseases in the Wider Caribbean. In Coral Health and Disease; Rosenberg, E., Loya, Y., Eds.; Springer: Berlin/Heidelberg, Germany, 2004; pp. 35–68. ISBN 978-3-662-06414-6. [Google Scholar]
  132. Garza-Perez, J.R.; Arias-González, J.E. Temporal change of a coral reef community in the south Mexican Caribbean. In Proceedings of the 52nd Gulf and Caribbean Fisheries Institute, Petersburg, FL, USA, 6–10 June 2001; Volume 52, pp. 415–427. [Google Scholar]
  133. Bruno, J.F.; Petes, L.E.; Harvell, C.D.; Hettinger, A. Nutrient enrichment can increase the severity of coral diseases. Ecol. Lett. 2003, 6, 1056–1061. [Google Scholar] [CrossRef]
  134. Mullen, K.M.; Harvell, C.D.; Alker, A.P.; Dube, D.; Jordán-Dahlgren, E.; Ward, J.R.; Petes, L.E. Host range and resistance to aspergillosis in three sea fan species from the Yucatan. Mar. Biol. 2006, 149, 1355–1364. [Google Scholar] [CrossRef]
  135. Ward, J.R.; Rypien, K.L.; Bruno, J.F.; Harvell, C.D.; Jordán-Dahlgren, E.; Mullen, K.M.; Rodríguez-Martínez, R.E.; Sánchez, J.; Smith, G. Coral diversity and disease in Mexico. Dis. Aquat. Organ. 2006, 69, 23–31. [Google Scholar] [CrossRef] [PubMed][Green Version]
  136. Jordán-Dahlgren, E.; Maldonado, M.A.; Rodríguez-Martínez, R.E. Diseases and partial mortality in Montastraea annularis species complex in reefs with differing environmental conditions (NW Caribbean and Gulf of México). Dis. Aquat. Organ. 2005, 63, 3–12. [Google Scholar] [CrossRef] [PubMed][Green Version]
  137. Foley, J.E.; Sokolow, S.H.; Girvetz, E.; Foley, C.W.; Foley, P. Spatial epidemiology of Caribbean yellow band syndrome in Montastrea spp. coral in the eastern Yucatan, Mexico. Hydrobiologia 2005, 548, 33–40. [Google Scholar] [CrossRef]
  138. Jordán-Garza, A.G.; Maldonado, M.A.; Baker, D.M.; Rodríguez-Martínez, R.E. High abundance of Diadema antillarum on a Mexican reef. Coral Reefs 2008, 27, 295. [Google Scholar] [CrossRef]
  139. Rodríguez-Martínez, R.E.; Banaszak, A.T.; Jordán-Dahlgren, E. Necrotic patches affect Acropora palmata (Scleractinia: Acroporidae) in the Mexican Caribbean. Dis. Aquat. Organ. 2001, 47, 229–234. [Google Scholar] [CrossRef] [PubMed]
  140. Álvarez-Filip, L.; Gil, I. Effects of Hurricanes Emily and Wilma on coral reefs in Cozumel, Mexico. Coral Reefs 2006, 25, 583. [Google Scholar] [CrossRef]
  141. Alvarez-Filip, L.; Encalada, M.; Reyes-Bonilla, H. Impact of Hurricanes Emily and Wilma on the Coral Community of Cozumel Island, Mexico. Bull. Mar. Sci. 2009, 84, 295–306. [Google Scholar]
  142. Alvarez del Castillo-Cárdenas, P.A.Á.; Reyes-Bonilla, H.; Alvarez-Filip, L.; Millet-Encalada, M.; Escobosa-González, L. Cozumel Island, México: A disturbance history. In Proceedings of the 11th International Coral Reef Symposium, Ft. Lauderdale, FL, USA, 7–11 July 2008; pp. 701–705. [Google Scholar]
  143. Fenner, D.P. Effects of Hurricane Gilbert on coral reefs, fishes and sponges at Cozumel, Mexico. Bull. Mar. Sci. 1991, 48, 719–730. [Google Scholar]
  144. Alvarez-Filip, L.; Dulvy, N.K.; Gill, J.A.; Côté, I.M.; Watkinson, A.R. Flattening of Caribbean coral reefs: Region-wide declines in architectural complexity. Proc. R. Soc. B Biol. Sci. 2009, 276, 3019–3025. [Google Scholar] [CrossRef][Green Version]
  145. Silva, R.; Mendoza, E.; Mariño-Tapia, I.; Martínez, M.L.; Escalante, E. An artificial reef improves coastal protection and provides a base for coral recovery. J. Coast. Res. 2016, 1, 467–471. [Google Scholar] [CrossRef]
  146. Calderón-Maya, J.R.; Orozco-Hernández, M.E. Planeación Y Modelo Urbano: El Caso De Cancún, Quintana Roo. Quivera 2009, 11, 18–34. [Google Scholar]
  147. Silva, R.; Oumeraci, H.; Martínez, M.L.; Chávez, V.; Lithgow, D.; Van Tussenbroek, B.I.; Van Rijswick, H.F.M.W.; Bouma, T.J. Ten Commandments for Sustainable, Safe, and W/Healthy Sandy Coasts Facing Global Change. Front. Mar. Sci. 2021, 8, 616321. [Google Scholar] [CrossRef]
  148. Chávez, V.; Lithgow, D.; Losada, M.; Silva-Casarin, R. Coastal green infrastructure to mitigate coastal squeeze. J. Infrastruct. Preserv. Resil. 2021, 2, 7. [Google Scholar] [CrossRef]
  149. European Commission; Eurostat. Towards Environmental Pressure Indicators for the EU; Publications Office: New York, NY, USA, 1999; ISBN 92-828-4978-3. [Google Scholar]
  150. Scharin, H.; Ericsdotter, S.; Elliott, M.; Turner, R.K.; Niiranen, S.; Blenckner, T.; Hyytiäinen, K.; Ahlvik, L.; Ahtiainen, H.; Artell, J.; et al. Processes for the sustainable stewardship of marine environments. Ecol. Econ. 2016, 128, 55–67. [Google Scholar] [CrossRef]
  151. Silva, R.; Martínez, M.L.; Van Tussenbroek, B.I.; Guzmán-rodríguez, L.O.; Mendoza, E.; López-portillo, J. A framework to manage coastal squeeze. Sustainability 2020, 12, 10610. [Google Scholar] [CrossRef]
  152. Morán, D.K.; De Paulo Salles, A.A.; Sánchez, J.C.; Espinal, J.C. Beach nourishment evolution in the Cancún Beach, Quintana Roo, México. In Proceedings of the 6th International Symposium on Coastal Engineering and Science of Coastal Sediment Processes, New Orleans, LA, USA, 13–17 May 2007; American Society of Civil Engineers (ASCE): Reston, VA, USA, 2007; pp. 2279–2291. [Google Scholar]
  153. Silva-Casarín, R.; Mariño-Tapia, I.; Enríquez-Ortiz, C.; Mendoza-Baldwin, E.; Escalante-Mancera, E.; Ruiz-Renteria, F. Monitoring shoreline changes at Cancun beach, Mexico: Effects of hurricane Wilma. In Proceedings of the 30th International Conference on Coastal Engineering, San Diego, CA, USA, 3–8 September 2006; American Society of Civil Engineers (ASCE): Reston, VA, USA, 2006; pp. 3491–3503. [Google Scholar]
  154. Escudero-Castillo, M.; Felix-Delgado, A.; Silva, R.; Mariño-Tapia, I.; Mendoza, E. Beach erosion and loss of protection environmental services in Cancun, Mexico. Ocean Coast. Manag. 2018, 156, 183–197. [Google Scholar] [CrossRef]
  155. Botero, C.; Pereira, C.; Tosic, M.; Manjarrez, G. Design of an index for monitoring the environmental quality of tourist beaches from a holistic approach. Ocean Coast. Manag. 2015, 108, 65–73. [Google Scholar] [CrossRef]
  156. Mendoza, E.; Silva, R.; Enriquez-Ortiz, C.; Mariño-Tapia, I.; Felix, A. Analysis of the Hazards and Vulnerability of the Cancun Beach System: The Case of Hurricane Wilma. In Extreme Events: Observations, Modeling, and Economics; Chavez, M., Ghil, M., Urrutia-Fucugauch, J., Eds.; American Geophysical Union: Washington, DC, USA, 2015; pp. 125–136. ISBN 9781119157052. [Google Scholar]
  157. González-Leija, M.; Mariño-Tapia, I.; Silva, R.; Enriquez, C.; Mendoza, E.; Escalante-Mancera, E.; Ruíz-Rentería, F.; Uc-Sánchez, E. Morphodynamic Evolution and Sediment Transport Processes of Cancun Beach. J. Coast. Res. 2013, 29, 1146–1157. [Google Scholar] [CrossRef]
  158. Hoegh-Guldberg, O. Climate change, coral bleaching and the future of the world’s coral reefs. Mar. Freshw. Res. 1999, 50, 839–866. [Google Scholar] [CrossRef][Green Version]
  159. Osorio-Cano, J.D.; Alcérreca-Huerta, J.C.; Mariño-Tapia, I.; Osorio, A.F.; Acevedo-Ramírez, C.; Enriquez, C.; Costa, M.; Pereira, P.; Mendoza, E.; Escudero, M.; et al. Effects of Roughness Loss on Reef Hydrodynamics and Coastal Protection: Approaches in Latin America. Estuaries Coasts 2019, 42, 1742–1760. [Google Scholar] [CrossRef]
Figure 1. The landscape metaphor for a bistable system. Pressure is the result of multiple disturbances (disturbance regime), and it increases if one or more disturbances increase in frequency or intensity. The blue circle (ball) follows the states of the system, which, depending on the disturbance regime, may move between troughs denoting the different stable states of the system. In the metaphor, stabilizing effects are likened to gravity, and stability is the result of the system’s tendency to move towards an attractor state, shown at the bottom of each basin. Adapted from [9].
Figure 1. The landscape metaphor for a bistable system. Pressure is the result of multiple disturbances (disturbance regime), and it increases if one or more disturbances increase in frequency or intensity. The blue circle (ball) follows the states of the system, which, depending on the disturbance regime, may move between troughs denoting the different stable states of the system. In the metaphor, stabilizing effects are likened to gravity, and stability is the result of the system’s tendency to move towards an attractor state, shown at the bottom of each basin. Adapted from [9].
Jmse 10 00644 g001
Figure 2. Flow of information through the different phases of the PRISMA framework.
Figure 2. Flow of information through the different phases of the PRISMA framework.
Jmse 10 00644 g002
Figure 3. Land use and land cover (LULC) in the Mexican Caribbean region. Data from [29,30].
Figure 3. Land use and land cover (LULC) in the Mexican Caribbean region. Data from [29,30].
Jmse 10 00644 g003
Figure 4. (a) Number of disturbance reports per year; (b) number of reports per disturbance type and ecosystem.
Figure 4. (a) Number of disturbance reports per year; (b) number of reports per disturbance type and ecosystem.
Jmse 10 00644 g004
Figure 5. Number of reports per ecosystem (represented by colours) for each type of disturbance (represented by the position of the circle) for the 11 municipalities in Quintana Roo. The size of the circle is proportional to the number of disturbances reported in each municipality.
Figure 5. Number of reports per ecosystem (represented by colours) for each type of disturbance (represented by the position of the circle) for the 11 municipalities in Quintana Roo. The size of the circle is proportional to the number of disturbances reported in each municipality.
Jmse 10 00644 g005
Figure 6. Disturbances reported in representative ecosystems of the Mexican Caribbean.
Figure 6. Disturbances reported in representative ecosystems of the Mexican Caribbean.
Jmse 10 00644 g006
Table 1. Disturbances reported for the Mexican Caribbean (Quintana Roo).
Table 1. Disturbances reported for the Mexican Caribbean (Quintana Roo).
EcosystemDisturbance CategoryDisturbance Type
RainforestAnthropogenicUrbanization
Land-use change to farming
Tree felling
Forest fires
Invasive species
Illegal hunting
Contaminant spill
Mass disposal of sargassum
NaturalHurricanes
Climate changeChanges in precipitation regimes
Rising temperature
Cenotes and Underground cave systemAnthropogenicGroundwater overexploitation
Tourism
Wastewater discharge
Leaching of contaminants
Leaching of sargassum
Climate changeChanges in precipitation regimes
Sea-level rise and saltwater intrusion
MangrovesAnthropogenicUrbanization
Tourism
Invasive species
Wastewater discharge
Dumping and burning of industrial and household waste
Mass disposal of sargassum
NaturalHurricanes
Climate changeSea-level rise and floods
Dunes and BeachesAnthropogenicUrbanization
Erosion
Mechanical beach cleaning
Excess noise
Installation of urban features and lighting
Invasive species
Wastewater discharge
NaturalHurricanes
Climate changeSea-level rise and floods
Rising air and sand temperature
Mass accumulation of sargassum
Seagrass meadowsAnthropogenicTouristic aquatic activities
Anchoring of vessels
Wastewater discharge
NaturalHurricanes
Overgrazing by turtles
Climate changeMass sargassum influx
Coral reefsAnthropogenicTouristic aquatic activities
Anchoring of boats
Marine traffic
Vessel groundings
Invasive species
Overfishing
Wastewater discharge
NaturalHurricanes
Infectious diseases
Climate changeRising seawater temperature
Ocean acidification
Coral bleaching
Mass sargassum influx
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Gómez, I.; Silva, R.; Lithgow, D.; Rodríguez, J.; Banaszak, A.T.; van Tussenbroek, B. A Review of Disturbances to the Ecosystems of the Mexican Caribbean, Their Causes and Consequences. J. Mar. Sci. Eng. 2022, 10, 644. https://doi.org/10.3390/jmse10050644

AMA Style

Gómez I, Silva R, Lithgow D, Rodríguez J, Banaszak AT, van Tussenbroek B. A Review of Disturbances to the Ecosystems of the Mexican Caribbean, Their Causes and Consequences. Journal of Marine Science and Engineering. 2022; 10(5):644. https://doi.org/10.3390/jmse10050644

Chicago/Turabian Style

Gómez, Izchel, Rodolfo Silva, Debora Lithgow, Janner Rodríguez, Anastazia Teresa Banaszak, and Brigitta van Tussenbroek. 2022. "A Review of Disturbances to the Ecosystems of the Mexican Caribbean, Their Causes and Consequences" Journal of Marine Science and Engineering 10, no. 5: 644. https://doi.org/10.3390/jmse10050644

Note that from the first issue of 2016, MDPI journals use article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop