*<IP_ADDRESS> Conventional non-image-guided surgical technique*

#### **Figure 5.**

*Anterior capsule opacification following multifocal intraocular lens implantation: the opacification of the remaining anterior capsule contributes in the reduction of potential optical phenomena.*

**111**

tion of a non-mIOL.

*Pseudophakic Presbyopic Corrections*

and dysphotopsia.

center [131].

*DOI: http://dx.doi.org/10.5772/intechopen.96528*

bimanual irrigation/aspiration.

• The nucleus is aspirated with or without ultrasound phacoemulsification energy according to the hardness of the crystalline lens, and residual cortex removal and posterior capsule polishing are performed using commonly

• The mIOL is always inserted into the capsular bag through the main incision. The IOL should be injected directly in the capsular bag in order a possibly traumatic surgical manoeuvre to be avoided. For this reason, adequate dilation

and an adequate capsulorrhexis of about 4.50 to 5.00 mm is necessary.

• For the optimal mIOL centration and the minimization of photic phenomena, especially for eyes with a large angle kappa, the mIOL is suggested to be decentered towards the visual axis, namely to be gently moved so as the microscope light reflex to fall within the central ring of the multifocal pattern [102]. This is an easy intraoperative manipulation that can effectively result in the desired centration on the visual axis. The centration of diffractive mIOLs on the visual axis is critical to their optimal performance. However, refractive mIOLs are also suggested to be centered on the visual axis because severe cases of decentration can increase the lens' effective power and induce astigmatism

• Additionally, since, normally, the visual axis is nasal to the optical center (the geometric center of the cornea, crystalline lens, and bag after nuclear and cortical removal), positioning the haptics of especially diffractive, but also refractive, IOLs at the 12 and 6 o'clock position may facilitate the desirable nasal displacement of the IOL optic. On the other hand, positioning the IOL haptics horizontally leads to the return of IOL to the geometrically horizontal

• To stabilize the mIOL centered on the visual axis during the first postoperative days, in contrast to the literature, the authors suggest that a minimal amount of cohesive ophthalmic viscosurgical device (OVD) could be left in the capsular bag without increasing the risk for elevation of the postoperative IOP [132].

• Since mIOL patients usually benefit from having a small pupil, eyes with a small pupil after the instillation of mydriatics before the cataract surgery should be managed with special caution in order the pupil to remain functionally and morphologically intact, as in its preoperative status. Therefore, it is strongly recommended to cataract refractive surgeons to avoid surgical maneuvers such as synechiolysis, pupil stretching, iris cutting [133] and the use of mechanical devices such as iris hooks and pupil expansion rings (e.g. Malyugin ring etc.) because of the high risk of intraoperative disruption of the pupillary sphincter and postoperative pupil enlargement [134]. Thus, intracameral administration of mydriatic agent, combined intracameral use of mydriatic agent and local anesthetic or the injection of OVD into the anterior chamber (viscomydriasis) should be preferred for the pupil dilation [134]. For an experienced refractive cataract surgeon, a possible threshold of pupil size for a successful phacoemulsification ranges between 4.5 and 5.0 mm [134, 135]. In smaller pupils which cannot be dilated pharmacologically or with OVD use, the surgeon should weigh the benefits and the risks of the pupil dilation with surgical maneuvres and mechanical devices and should consider the implanta-

### *Pseudophakic Presbyopic Corrections DOI: http://dx.doi.org/10.5772/intechopen.96528*

*Current Cataract Surgical Techniques*

following practices are suggested:

of iodine povidone.

surgical technique, will be discussed in the text below.

*<IP_ADDRESS> Conventional non-image-guided surgical technique*

(commonly 2.2-mm) cataract surgery.

of parameters for the conventional non-image-guided, but also for an image-guided

• Topical anesthesia and mydriatic drops are instilled before the operation.

• Periorbital skin, eyelids, and the conjunctival sac are prepared with a solution

• The surgical technique is performed using a standard technique of sutureless

• Intracameral anesthesia and potentially intracameral mydriatics are injected.

• Capsulorrhexis should have a diameter between 4.50 to 5.00 mm. Although a diameter larger than 5.00 mm also is recommended to facilitate nuclear and cortical removal, this increases the risk of postoperative optical phenomena caused by the involvement of more concentric rings when the light rays pass through the IOL's optic. Opacification of the remaining anterior capsule can reduce optical phenomena even in eyes with a pupil diameter larger than 5.00 mm (**Figure 5**).

 The capsulorrhexis is suggested to be centered around the microscope light reflection on the anterior capsule (patients' visual axis) rather than around the pupillary axis [131]. However, in the case of a mature cataract where the patient fails to fixate on the microscope light, but also on the lights of the biometry device during the preoperative examination, the implantation of a mIOL should be avoided, since the risk for a decentered implantation is very high. The centration on the pupil center or on the geometric center of the cornea is not considered as a safe alternative solution.

*Anterior capsule opacification following multifocal intraocular lens implantation: the opacification of the*

*remaining anterior capsule contributes in the reduction of potential optical phenomena.*

For the best possible refractive outcome during mIOL implantation surgery, the

**110**

**Figure 5.**

• Videorecording of every surgery is suggested for refractive cataract surgeons and, generally, for ophthalmic surgeons in order to review their surgeries, criticize their technique, find mistakes that should have been avoided, explain unexpected outcomes and improve their surgical skills [136].

#### *<IP_ADDRESS> Image-guided surgery*

Although the experience and the surgical skills of the refractive cataract surgeon play the most significant role in the final refractive outcome, image-guided lens extraction surgery, which has been recently introduced in phacoemulsification, can increase the surgical accuracy, decrease the risk of complications such as postoperative astigmatism, IOL decentration and photopic phenomena and improve the patient's quality of vision [41].

Image-guided systems such as Verion Digital Marker (Alcon Laboratories, Inc., Fort Worth, TX, USA) [137] and Zeiss Callisto Eye (Carl Zeiss AG, Dublin, CA) [138] are commonly used for the implantation of multifocal toric IOLs. However, since the high accuracy is also necessary during the implantation of multifocal non-toric IOLs for main and sideport incisions, the centration and the diameter of capsulorrhexis, as well as for the centration of the mIOL implantation, the authors suggest that digital image-guidance also during the implantation of multifocal non-toric IOLs could optimize the surgical accuracy and predictability, minimize the risk of complications, and maximize the refractive outcome. **Figure 6** presents the basic steps of lens extraction surgery (a. sideport incisions, b. main incision, c. capsulorrhexis, d. IOL centration, e. finalization) using the Verion image-guided system during the implantation of a multifocal non-toric IOL.

#### *3.2.4 Complications*

Implantation of mIOLs provide patients with a good visual acuity at more than one focal point depending on mIOL design. Patient satisfaction levels after mIOL implantation are high. However, the same characteristics that offer refractive correction at all distances can result in adverse effects at the same time [98].

For instance, light distribution mechanisms split the light to two or three focal points. As a result, less amount of light from each focal point reaches the retina worsening the contrast sensitivity, especially in mesopic light conditions [98, 139]. Therefore, two or three distinct images are produced, one sharp on focus and one blurred out of focus. The light of the latter image reduces the detectability of the on-focus image, resulting in the lower contrast sensitivity, however within the normal range of age-matched phakic individuals, and in the creation of dysphotopic phenomena such as halos [139–141]. These phenomena commonly diminish over time through the process of neuroadaptation.

The most common reason for patient dissatisfaction is *blurred vision* (approximately in 95% of the dissatisfied patients) caused by residual ametropia/astigmatism [98] or posterior capsular opacification (PCO), [97] although these subjective complains usually do not correspond to the objective VA [98, 142]. An additional cause of dissatisfaction is *dysphotopsia*, which is caused by the IOL itself or/and by a potential IOL decentration or IOL tilt or/and by a large pupil diameter. Refractive mIOLs appear to be related with higher levels of photic phenomena than diffractive mIOLs [143, 144]. Moreover, the existence of *dry eye disease* postoperatively found to be one of the patient complaints resulting in symptoms of discomfort, visual disturbance, and tear-film instability. Finally, *IOL explantation* has been reported in

**113**

perception [148].

**Figure 6.**

*3.3.1 Accommodative IOLs*

distances [149].

*Pseudophakic Presbyopic Corrections*

*DOI: http://dx.doi.org/10.5772/intechopen.96528*

a frequency between 0.85% and 7 % [98, 145, 146] due to IOL dislocation, refractive error, PCO, failure to neuroadaptation [147] and, rarely, loss of normal color

*The basic steps of multifocal IOL implantation using the Verion image-guided system ((a) sideport incisions,*

Apart from monovision technique with bilateral implantation of monofocal IOLs and bilateral implantation of multifocal IOLs, accommodative and EDOF IOL, as well as a combination of different IOL types and designs are some new alternative solutions of pseudophakic presbyopic correction. However, these options are beyond the scope of this chapter and they will not be analytically described.

Accommodative IOLs (aIOLs) are designed to simulate the mechanism of accommodation of the crystalline lens, which is capable of changing dynamically its dioptric power with accommodating effort, namely by modifying its shape after contraction of the ciliary muscle and providing functional vision at different

**3.3 New IOL technologies for presbyopic correction**

*(b) main incision, (c) capsulorrhexis, (d) IOL centration, (e) finalization).*

*Pseudophakic Presbyopic Corrections DOI: http://dx.doi.org/10.5772/intechopen.96528*

*Current Cataract Surgical Techniques*

*<IP_ADDRESS> Image-guided surgery*

patient's quality of vision [41].

non-toric IOL.

*3.2.4 Complications*

• Videorecording of every surgery is suggested for refractive cataract surgeons and, generally, for ophthalmic surgeons in order to review their surgeries, criticize their technique, find mistakes that should have been avoided, explain

Although the experience and the surgical skills of the refractive cataract surgeon

play the most significant role in the final refractive outcome, image-guided lens extraction surgery, which has been recently introduced in phacoemulsification, can increase the surgical accuracy, decrease the risk of complications such as postoperative astigmatism, IOL decentration and photopic phenomena and improve the

Image-guided systems such as Verion Digital Marker (Alcon Laboratories, Inc., Fort Worth, TX, USA) [137] and Zeiss Callisto Eye (Carl Zeiss AG, Dublin, CA) [138] are commonly used for the implantation of multifocal toric IOLs. However, since the high accuracy is also necessary during the implantation of multifocal non-toric IOLs for main and sideport incisions, the centration and the diameter of capsulorrhexis, as well as for the centration of the mIOL implantation, the authors suggest that digital image-guidance also during the implantation of multifocal non-toric IOLs could optimize the surgical accuracy and predictability, minimize the risk of complications, and maximize the refractive outcome. **Figure 6** presents the basic steps of lens extraction surgery (a. sideport incisions, b. main incision, c. capsulorrhexis, d. IOL centration, e. finalization) using the Verion image-guided system during the implantation of a multifocal

Implantation of mIOLs provide patients with a good visual acuity at more than one focal point depending on mIOL design. Patient satisfaction levels after mIOL implantation are high. However, the same characteristics that offer refractive cor-

For instance, light distribution mechanisms split the light to two or three focal points. As a result, less amount of light from each focal point reaches the retina worsening the contrast sensitivity, especially in mesopic light conditions [98, 139]. Therefore, two or three distinct images are produced, one sharp on focus and one blurred out of focus. The light of the latter image reduces the detectability of the on-focus image, resulting in the lower contrast sensitivity, however within the normal range of age-matched phakic individuals, and in the creation of dysphotopic phenomena such as halos [139–141]. These phenomena commonly diminish over

The most common reason for patient dissatisfaction is *blurred vision* (approximately in 95% of the dissatisfied patients) caused by residual ametropia/astigmatism [98] or posterior capsular opacification (PCO), [97] although these subjective complains usually do not correspond to the objective VA [98, 142]. An additional cause of dissatisfaction is *dysphotopsia*, which is caused by the IOL itself or/and by a potential IOL decentration or IOL tilt or/and by a large pupil diameter. Refractive mIOLs appear to be related with higher levels of photic phenomena than diffractive mIOLs [143, 144]. Moreover, the existence of *dry eye disease* postoperatively found to be one of the patient complaints resulting in symptoms of discomfort, visual disturbance, and tear-film instability. Finally, *IOL explantation* has been reported in

rection at all distances can result in adverse effects at the same time [98].

time through the process of neuroadaptation.

unexpected outcomes and improve their surgical skills [136].

**112**

#### **Figure 6.**

*The basic steps of multifocal IOL implantation using the Verion image-guided system ((a) sideport incisions, (b) main incision, (c) capsulorrhexis, (d) IOL centration, (e) finalization).*

a frequency between 0.85% and 7 % [98, 145, 146] due to IOL dislocation, refractive error, PCO, failure to neuroadaptation [147] and, rarely, loss of normal color perception [148].

#### **3.3 New IOL technologies for presbyopic correction**

Apart from monovision technique with bilateral implantation of monofocal IOLs and bilateral implantation of multifocal IOLs, accommodative and EDOF IOL, as well as a combination of different IOL types and designs are some new alternative solutions of pseudophakic presbyopic correction. However, these options are beyond the scope of this chapter and they will not be analytically described.

#### *3.3.1 Accommodative IOLs*

Accommodative IOLs (aIOLs) are designed to simulate the mechanism of accommodation of the crystalline lens, which is capable of changing dynamically its dioptric power with accommodating effort, namely by modifying its shape after contraction of the ciliary muscle and providing functional vision at different distances [149].

AIOLs are still a developing field in the technology of premium IOLs where a variety of designs are still examined [150]. The mechanisms of action of the different types of aIOLs that are currently available are based on the three following principles: (a) change in axial position (i. single-optic aIOLs, and ii. dual-optic aIOLs), (b) change in shape or curvature, and (c) change in refractive index or power. Apart from the aforementioned aIOL designs, the following new design strategies of aIOLs, still in preclinical stage, have been proposed: (i) lens-filling aIOL techniques, and (ii) electroadaptive aIOLs [149, 151]. Another issue that remains to be solved is the best location for implantation of aIOLs. Implantation inside the capsular bag seem to be a less successful approach in comparison to the sulcus, since in sulcus, the dynamics from the ciliary body induce further movements of the IOL [149, 150].

Despite the significant development and evolution of aIOLs and the great variety of IOL designs, the majority of them are still in a development process and have shown some contradictory clinical data about their efficacy. The optimal aIOL with a broad range of accommodation still remains elusive, and different challenges exist for each lens design. However, new innovative and promising designs and technologies now exist having the restoration of accommodation as their common goal [149, 151].

## *3.3.2 Extended depth-of-focus (EDOF) IOLs*

Extended depth-of-focus (EDOF) IOL is a new technology in the treatment of presbyopia-correcting IOLs. The basic optical principle of EDOF IOLs is to create a single elongated focal point, in contrast to monofocal IOLs, in which light is focused on one single point, and mIOLs, in which light is focused on two or three discrete points (**Figure 7**). In this way, EDOF IOLs eliminate the overlapping of far and near images caused my mIOLs, thus eliminating the halo effect. Specifically, EDOF IOLs provide a continuous focus range that extends from the far focus area until the intermediate distance, without the clearly asymmetric IOL power distribution that is provided by the mIOLs. In this way, EDOF IOLs avoid the presence of secondary out-of-focus images that originates the halos [152–154].

The idea of EDOF was first reported in 1984 by Nakazawa and Ohtsuki who measured an apparent 2.00 D accommodation in 39 pseudophakic eyes implanted with posterior chamber spherical IOLs and found a significant correlation between apparent accommodation and depth of field. This correlation was inversely proportional to the pupillary diameter [155]. After using multiple cornea- or IOL-based strategies, the first EDOF IOL (Symfony, Johnson and Johnson Vision, Jacksonville, FL) was introduced into the market receiving the European Economic Area

**115**

*Pseudophakic Presbyopic Corrections*

*DOI: http://dx.doi.org/10.5772/intechopen.96528*

Drug Administration (FDA) in July 2016 [156].

certification mark in June 2014, and being approved by the United States Food and

Since then, a variety of EDOF-labeled IOLs have been released in the market and are based on the following 3 optical models: i) spherical aberration, ii) chromatic aberration, iii) pinhole effect, all of which allow obtaining greater depth of focus [157]. Apart from the pure EDOF IOLs, there are some IOLs that combine multifocality with low addition power and the EDOF technology, the so-called "hybrid IOLs" [157]. In general, EDOF IOLs provide better optical quality in comparison with monofocal and multifocal IOLs [158–160] Additionally, EDOF IOLs provide high uncorrected intermediate vision, but inadequate near vision [161, 162], thus allowing a relative spectacle independence. A potential disadvantage of EDOF-IOLs is a decreased quality of retinal image if the aberrations are excessively increased. Finally, contrast sensitivity, glare and halos vary depending on the EDOF-IOL technology, however, they seem to be better when compared to mIOLs. [163] Since the literature results about the optical performance of EDOF-IOLs are promising but contraindicating, [164–166] new large-scale studies need to be performed.

In any case, patients should be counseled about potential photic phenomena and the need for low power reading spectacles postoperatively. Moreover, the IOL type

When a large anisometropia is targeted for an optimal near visual acuity, pseudophakic monovision with implantation of monofocal IOLs results in a relative decrease in near stereopsis [49, 153]. Therefore, a new type of monovision with implantation of different IOL types and IOL technologies in each eye has been introduced. For instance, the implantation of a monofocal IOL in the dominant eye and a premium lens such as mIOL (bifocal or trifocal/refractive, diffractive or hybrid diffractive-refractive) [167, 168] or EDOF IOL in the recessive one, the so-called "hybrid monovision" or "mix and match" or "blended vision", has been applied and compared with the conventional myopic monovision techniques and with the binocular implantation of premium IOLs showing promising visual outcomes [153, 154, 169]. Additionally, the use of a refractive IOL in the dominant eye and a diffractive IOL in the recessive eye [170] or vice versa [171] has been reported showing very good visual outcomes including impressive spectacle independence at all distances and a contrast sensitivity being comparable with phakic patients. In general, it seems that hybrid monovision offers spectacle-free postoperative visual

Apart from the full preoperative examination and the high-precision surgery that are necessary for optimal refractive outcomes in patients undergoing a pseudophakic presbyopic correction, especially with mIOLs, the postoperative follow-up plays an equally significant role in the best possible results. The most common follow-up timepoints are 1 day, 1 week, 1 month, 3 months, 6 months, 1 year, 2 years and so forth. Examination at the first postoperative day is commonly applied by many surgeons, However, the current literature supports that first-day examination after an uneventful phacoemulsification surgery is not necessary when patients have not posterior synechiae or chronic/recurrent uveitis and they are operated by experienced cataract surgeons. Thus, healthcare costs can be decreased without an

decision should be made depending on their profile and preferences.

*3.3.3 Monovision techniques with combination of IOLs*

capacity at all distances with minimal optical phenomena.

**4. Postoperative examination – follow-up**

increased risk to the patients [172].

**Figure 7.** *EDOF IOL design.*

#### *Pseudophakic Presbyopic Corrections DOI: http://dx.doi.org/10.5772/intechopen.96528*

*Current Cataract Surgical Techniques*

ments of the IOL [149, 150].

*3.3.2 Extended depth-of-focus (EDOF) IOLs*

out-of-focus images that originates the halos [152–154].

AIOLs are still a developing field in the technology of premium IOLs where a variety of designs are still examined [150]. The mechanisms of action of the different types of aIOLs that are currently available are based on the three following principles: (a) change in axial position (i. single-optic aIOLs, and ii. dual-optic aIOLs), (b) change in shape or curvature, and (c) change in refractive index or power. Apart from the aforementioned aIOL designs, the following new design strategies of aIOLs, still in preclinical stage, have been proposed: (i) lens-filling aIOL techniques, and (ii) electroadaptive aIOLs [149, 151]. Another issue that remains to be solved is the best location for implantation of aIOLs. Implantation inside the capsular bag seem to be a less successful approach in comparison to the sulcus, since in sulcus, the dynamics from the ciliary body induce further move-

Despite the significant development and evolution of aIOLs and the great variety

Extended depth-of-focus (EDOF) IOL is a new technology in the treatment of presbyopia-correcting IOLs. The basic optical principle of EDOF IOLs is to create a single elongated focal point, in contrast to monofocal IOLs, in which light is focused on one single point, and mIOLs, in which light is focused on two or three discrete points (**Figure 7**). In this way, EDOF IOLs eliminate the overlapping of far and near images caused my mIOLs, thus eliminating the halo effect. Specifically, EDOF IOLs provide a continuous focus range that extends from the far focus area until the intermediate distance, without the clearly asymmetric IOL power distribution that is provided by the mIOLs. In this way, EDOF IOLs avoid the presence of secondary

The idea of EDOF was first reported in 1984 by Nakazawa and Ohtsuki who measured an apparent 2.00 D accommodation in 39 pseudophakic eyes implanted with posterior chamber spherical IOLs and found a significant correlation between apparent accommodation and depth of field. This correlation was inversely proportional to the pupillary diameter [155]. After using multiple cornea- or IOL-based strategies, the first EDOF IOL (Symfony, Johnson and Johnson Vision, Jacksonville,

FL) was introduced into the market receiving the European Economic Area

of IOL designs, the majority of them are still in a development process and have shown some contradictory clinical data about their efficacy. The optimal aIOL with a broad range of accommodation still remains elusive, and different challenges exist for each lens design. However, new innovative and promising designs and technologies now exist having the restoration of accommodation as their common goal [149, 151].

**114**

**Figure 7.** *EDOF IOL design.* certification mark in June 2014, and being approved by the United States Food and Drug Administration (FDA) in July 2016 [156].

Since then, a variety of EDOF-labeled IOLs have been released in the market and are based on the following 3 optical models: i) spherical aberration, ii) chromatic aberration, iii) pinhole effect, all of which allow obtaining greater depth of focus [157]. Apart from the pure EDOF IOLs, there are some IOLs that combine multifocality with low addition power and the EDOF technology, the so-called "hybrid IOLs" [157]. In general, EDOF IOLs provide better optical quality in comparison with monofocal and multifocal IOLs [158–160] Additionally, EDOF IOLs provide high uncorrected intermediate vision, but inadequate near vision [161, 162], thus allowing a relative spectacle independence. A potential disadvantage of EDOF-IOLs is a decreased quality of retinal image if the aberrations are excessively increased. Finally, contrast sensitivity, glare and halos vary depending on the EDOF-IOL technology, however, they seem to be better when compared to mIOLs. [163] Since the literature results about the optical performance of EDOF-IOLs are promising but contraindicating, [164–166] new large-scale studies need to be performed.

In any case, patients should be counseled about potential photic phenomena and the need for low power reading spectacles postoperatively. Moreover, the IOL type decision should be made depending on their profile and preferences.


Subterranean Waters in Riviera Maya of the Yucatan Peninsula: Vulnerability and the Importance of Monitoring

*Luis M. Mejía-Ortíz, Alejandro L. Collantes-Chávez-Costa, Cruz López-Contreras and Oscar Frausto-Martínez*

## **Abstract**

The Mexican Caribbean coast has great scenic beauty both on the surface and underwater, which is why it has been a developing area for tourism since the 1970s, establishing sites such as Cancun and Playa del Carmen and empowering others such as Cozumel and Tulum. Their biological richness is enormous, especially in the Mesoamerican Reef of which they are a part. However, this richness and scenic beauty are not possible without the ecological assemblages that exist within these regions' adjacent ecosystems, mainly the surrounding seasonally dry tropical forest and the coastal wetlands that, together with the oceanographic characteristics of the Caribbean Sea, potentiate it, turning the region into the most visited in Latin America. To this end, groundwater plays a very important role in the assemblages of biotic and abiotic elements that are shared with the Caribbean Sea; thus, its constant monitoring allows us to identify how the changes that occur in the tropical forest are producing various changes in the composition and abundance of coastal reef elements. Here, we present results of our study of groundwater conditions (temp, pH, oxygen dissolved, and salinity) in nineteen cenotes and underground rivers of the Riviera Maya and six cenotes of Cozumel. We also profiled the predominant vegetation on the surface of this region, which is a seasonally dry tropical forest, to understand the components and functioning of these subterranean ecosystems to assess their vulnerability and identify their threats from human development (population growth, tourism development, mobility capacity). These threats not only affect the cave and coastal organisms but also the tropical karstic landscapes that are characteristic of these systems.

**Keywords:** underground, aquatic monitoring, ecological links, vulnerability

## **1. Introduction**

The groundwaters in many places around the world are sources of freshwater for human use [1]. In Mexico, the Yucatan Peninsula is the largest freshwater source in the region. Its soil is mainly karstic, allowing a high porosity and filtration of rainwater to the underground [2, 3]. Due to this reservoir, the tropical forest is tall and exuberant because the soil layer is thin enough to allow tree roots to reach the aquifer. The extreme hot conditions cause the forest to be dry or semi-dry [4, 5]. Over many years, these conditions have produced thousands of conduits and entrances [6, 7] that reach to coastal areas as subterranean rivers. The richness of the Caribbean Sea establishes important conditions for the proliferation of coral reefs [8]. The terrestrial ecosystems (tropical forest, mangrove, and dune) are connected by underground waters that establish links among the adjacent terrestrial and marine ecosystems (coastal lagoons, sea grass, and coral reefs). However, this role that is important, has been poorly valuation, and the groundwaters has a unique characteristics that produce a special ecosystems [9]. The state of Quintana Roo and its coast have natural attractions with unique scenic beauty, such as Caribbean beaches, reefs, lagoons, and archeological sites, among others. Tourism is based on sun and sand, but there are other tourist attractions that are highly visited, such as nature reserves and cultural areas [10]. This set of attractions motivated the creation of Cancún in 1970, which became the largest and most important tourist destination in Mexico and the Caribbean [11]. Natural attractions also led to the development of the Riviera Maya in the 1990s, which is equally as recognized as Cancun [12]. Together, these locations receive around 12 million visitors per year [13]. Initially, tourists visited for the coastal and marine landscape, but in recent years visitors have become more interested in the cenotes and underground activities. All these, therefore that another human activity such as mobility, pork farms, soil extractions and growing of the cities are the development project that in the next years will produce environmental impacts in special to water [14]. For these reasons, it is important to monitor the water to understand how the ecosystems work.

#### **2. Material and methods**

From 2016 to 2020, we profiled 19 cenotes in Riviera Maya and six in Cozumel (**Figure 1**) using the Hydrolab Data Sonde 5 (Hydrolab DS5) to identify the different layers and variations. We recorded dissolved oxygen (±0.01 mg/l), pH (±001 pH), salinity (±0.01%), and water temperature (±0.01°C). The Hydrolab DS5 was programed to record every 30 seconds and the divers introduce in the cave during one and half hours. At the same time, recording of faunal composition was conducted to identify crustaceans such as isopods, different species of shrimp, amphipods, and remipedes [15–17]. Divers also recorded tree roots into the aquifer using taxonomic guides [18, 19] and identified the systems with clear water discharges to the Caribbean Sea. We also examined tourism and tourist activities in the Riviera Maya and Cozumel and corroborated this data with vegetation and soil use in the surrounding the cenotes as well as with data reported in the literature.

#### **3. Results**

#### **3.1 Environmental conditions**

After checking the profiles of twenty-four underground systems, it was possible to recognize three main ecosystems. The first is a freshwater ecosystem that is not stratified and that has similar conditions of oxygen, temperature, and pH in superficial

*DOI: http://dx.doi.org/10.5772/intechopen.106437 Subterranean Waters in Riviera Maya of the Yucatan Peninsula: Vulnerability...*

#### **Figure 1.**

*Location of the different cenotes in the Riviera Maya and Cozumel.*

and bottom areas. We recorded 10 sites in freshwater ecosystems (**Table 1**), some of which are shallow ponds and some of which are 15 meters deep.

In these profiles, the water column is not stratified accordingly with the salinity content. The temperature and oxygen dissolved have a negative relationship with the depth because both variables decrease as depth increases. However, pH values are more independent and showed variations, possibly due to the biochemical karst process, as has been reported for other systems [20] (**Figure 2**).

The second type of ecosystem is a brackish/marine water ecosystem. In these ecosystems the marine entrance has a direct connection with the sea. As such, some marine animals such as echinoderms and some species of fish live in caves. In these systems the mixing zone between freshwater and marine water is all time and only in some season is possible identify stratification in the water column. We recorded two systems in this study (**Figure 3** and **Table 2**).

The third type of ecosystem is an anchialine pool, which is a subterranean estuary containing freshwater and marine water separated by a mixing zone called the halocline. Anchialine pools can be found at different depths according to their distance from the sea. In this study, we recorded thirteen of these systems in the Riviera Maya and Cozumel. In these ecosystems, the stratified water column is due to the salinity changes that produce similar conditions of temperature, pH, and oxygen dissolved. It is interesting that in these environments the most rich species were found just past the halocline in the marine layer.

In anchialine ecosystems the temperature and oxygen dissolved decrease as depth increases, and both have a direct relationship with the halocline at different depths.

*DOI: http://dx.doi.org/10.5772/intechopen.106437 Subterranean Waters in Riviera Maya of the Yucatan Peninsula: Vulnerability...*

#### **Figure 2.**

*Examples of profiles according to the depth of freshwater ecosystems. A, B, and C graphs are for the Santa Cruz system, and D, E, and F graphs are for the Vaca ha system. Salinity is represented by continuum lines with* □*, and temperature, oxygen dissolved, and pH are represented by dashed lines with •.*

However, in the case of Cenote Calavera, the temperature increases at same time that the marine layer is present. In contrast, the pH values in all cenotes are higher in comparison with the superficial layer due to the alkalinity value of the marine layer (**Figure 4**).

These three main ecosystems exist in different places according with several factors such as surrounding vegetation but mainly with the depth when the subterranean branch cave reaches, but also is relationship with the distance from the coast that the cenote (entrance) is located because the incorporation of the marine layer is most important in the those systems close to the coastal area but far away to the coastal line the freshwater lenses is more wider whilst that the marine layer is found to deeper area (**Figure 5**).

#### **3.2 Surrounding vegetation to the aquifer**

The semi-evergreen seasonal forest is the dominant tropical forest in the study area, and in the state of Quintana Roo [21, 22]. In Mexico, this kind of seasonal

#### **Figure 3.**

*Examples of profiles of brackish/marine ecosystems according to diving time. A, B, and C graphs are for casa cenote from the Actun ha system, and D, E, and F graphs are for cenote Aerolito in Cozumel. Salinity is represented by continuum lines, and temperature, oxygen dissolved, and pH are represented by dashed lines with •.*

**Table 2.**

*Record of brackish/marine water subterranean ecosystems with environmental conditions and fauna registered.*

tropical forest is known as a tropical evergreen forest [23] or medium semi-evergreen forest [24]. This vegetation develops in the *Aw* climate [25], characterized by a short but well-marked dry season, which in the area extends from November to May, during which short, sporadic, and infrequent rains may occur (191 mm in average), in addition to a rainy season the rest of the year, with rainfall around 1000 mm and an average annual temperature between 20 and 25°C. A semi-evergreen seasonal tropical forest grows on mainly flat terrain with shallow soils (20 or 35 cm deep), generally of the Rendzina type, and with outcrops of limestone [4].

*DOI: http://dx.doi.org/10.5772/intechopen.106437 Subterranean Waters in Riviera Maya of the Yucatan Peninsula: Vulnerability...*

#### **Figure 4.**

*Examples of profiles according to the depth of the water column of anchialine ecosystems. A, B, and C graphs are for cenote Calavera, and D, E, and F graphs are for cenote Chempita in Cozumel. Salinity is represented by continuum lines with* □*, and temperature, oxygen dissolved, and pH are represented by dashed lines with •.*

Although a large area of this tropical seasonal forest is currently secondary, relics of the original forest can still be found [26]. Several tree strata define its vertical structure with the abundant presence of climbers and epiphytes and a well-developed shrub layer as well as an herbaceous layer composed of seedlings from the species at the upper strata [18]. The characteristic tree species are *Bursera simaruba* (L.) Sarg., *Metopium rownie* (Jacq.) Urb., *Vitex gaumeri* Greenm., *Brosimum alicastrum* Sw., *Manilkara zapota* (L.) P. Royen, and *Psidium sartorianum* (O.Berg) Nied. Among the most frequent shrubs are *Acacia collinsi* Saff., *Bauhinia jenningsii* P. Wilson, and *Eugenia acapulcensis* Steud. To name a few. In the epiphytic stratum, there are species such as *Brassavola nodosa* (L.) Lindl. And *Selenicereus testudo* (Karw. Ex Zucc.) Buxb.

The height of trees in the semi-evergreen seasonal tropical forest ranges from 18 to 25 m [24]. Trees of up to 35 m can also be found [4]; these are associated with better environmental conditions [18] such as areas with greater soil depth and karst water bodies (cenotes). The vegetation associated with these cenotes has the same floristic composition of the semi-evergreen seasonal tropical forest, but the tree stratum shows to be characteristically evergreen with a greater abundance of epiphytes (**Figure 6**) [4, 19].

#### *Limnology - The Importance of Monitoring and Correlations of Lentic and Lotic Waters*

#### **Figure 5.**

*Schematic underwater profile where it is possible to see the relationship (halocline) between freshwater (light blue) and marine (dark blue) layers, according to depth and distance from the sea. The tree roots that reaching the aquifer to maintained the semi-evergreen state of tropical forest and mangrove vegetation.*

#### **4. Discussion**

#### **4.1 Tourist activity in the cenotes and its impacts**

The great diversity and scenic beauty of the Riviera Maya, both on the surface and underwater, is related to the different types of ecosystems and large amounts of natural resources. This has facilitated the diversification of tourist activity, which now also includes exploring underground rivers, cenotes, and caves [27].

Visits to cenotes have increased significantly. The arrival of sargassum on the coast of Quintana Roo has motivated visitors to move to these spaces [28], since tourism service providers have recognized them as a substitute for beaches.

The cenotes have great landscape and cultural importance. Their underwater landscapes are geologically sculptural, which, together with their link to the general Mayan culture, creates a synergy in the visit. The cultural importance of cenotes dates *DOI: http://dx.doi.org/10.5772/intechopen.106437 Subterranean Waters in Riviera Maya of the Yucatan Peninsula: Vulnerability...*

**Figure 6.** *Vegetation type and land use for the study area.*

to pre-Hispanic times, and rituals and offerings learned from their Mayan ancestors are still performed these days to request rain, care for crops, and to ask for permission to enter the cenote [29]. Cenotes contain unique fauna and flora, formations such as stalagmites and stalactites, and ritual elements of the Mayan civilization. In addition, the areas around the cenotes are usually surrounded by jungle, mangrove, or palm and with different species of fauna that give each site an evocative power. This is why it is in these areas that observation and interpretation walks of the Mayan culture are offered.

The cenotes not only have unique esthetic natural characteristics that entice people to visit them, but they are also repositories of unique species of flora and fauna, which is where the biological and ecological importance of these systems lies [30]. Although cenotes are highly fragile ecosystems, there are currently no regulations for their use and management. In addition, since they are not isolated systems but rather they connect with groundwater that sometimes connects with the sea [31], their inappropriate use can cause unquantifiable impacts on the rest of the ecosystems with which they interact [28].

The excess of tourists in the cenotes is putting the aquifer and its aquatic biota at risk. Visitors introduce physical, chemical, and biological agents into the cenotes, such as garbage, sunscreens, repellents, creams, and fecal matter. These contaminants can alter the system, causing changes in temperature, erosion, increase in fecal coliforms, and excess nutrients that can generate irreversible impacts [27, 28]. Several of the cenotes studied experience high tourist activity (**Table 1**) because they are being offered as recreational spaces for swimming, snorkeling, diving, and hiking.

#### *DOI: http://dx.doi.org/10.5772/intechopen.106437 Subterranean Waters in Riviera Maya of the Yucatan Peninsula: Vulnerability...*

The three ecosystem types discussed have a strong relationship with the dynamics of tropical dry forest function, especially in those that are far away from the coast. However, these relationships also exist in coastal areas where the vegetation type is characterized by mangrove and dune. How as been reported to terrestrial cave environments they are not isolated and in these cases the cave systems fully of water have interesting relationship with the out ecosystems surrounding [32]. The freshwater from the aquifer in Quintana Roo is one of the best-conserved reservoirs in the country, but at same time it faces several threats. Exponential population growth has occurred in Playa del Carmen, Tulum, Puerto Morelos, Akumal, Cozumel, and Puerto Aventuras, thus increasing demand for water. Tourism activity is changing from sun and beach activities to activities in the cenotes and adjacent ecosystems, especially the dry tropical forest [14]. This transition in tourism increases the threat to all underground systems because these new activities cause pollution by dissolved agents and solid wastes, as has been reported by several local organizations [33].

**Table 4.** *Tourist activity in cenotes.*

This region is experiencing a continual increase in tourism and mobility infrastructure [10] that together with the water demands evidently change the underground water conditions because exist the risk that if the pumping water increase the marine layer occupied these subterranean spaces and this work show the first photograph of these ecosystems under study which, possibly in one or two decades will be change. All these threats are present due to the economic benefits of tourist activity in the area. The different options to diminish the damage include environmental instruments and laws established by institutions such as the Federal Attorney for Environmental Protection (PROFEPA), Secretariat of Environment and Natural Resources (SEMARNAT), and National Commission of Natural Protected Areas Mexico (CONANP). Some proposed actions to reduce the harmful impacts of increased tourism include wastewater treatments, avoiding developing artificial greens like golf courses, stadiums, and parks, forbidding the injection of wastewater to deeper aquifers, and environmental education.

The discussed ecosystems are facing natural and anthropogenic impacts, highlighting their vulnerability. As such, monitoring their water conditions is highly important (**Tables 3** and **4**).

### **5. Conclusions**

This chapter presented results of our study of groundwater conditions (temp, pH, oxygen dissolved, and salinity) in nineteen cenotes and underground rivers of the Mexican Caribbean corridor from Tulum to Puerto Morelos (Riviera Maya, Yucatan Peninsula) and six cenotes of Cozumel. We also profiled the predominant vegetation on the surface of this region, which is a seasonally dry tropical forest, to understand the components and functioning of these subterranean ecosystems to assess their vulnerability and identify their threats from human development (population growth, tourism development, mobility capacity). We identified three types of underground aquatic ecosystems: freshwater, brackish/marine water, and anchialine.

Rapid growth in tourism in the Riveria Maya and Cozumel, among other locations, is polluting and contaminating these regions' ecosystems and thus it is of great importance to monitor these ecosystems and the fauna that inhabit them to identify their capacity for resilience.

#### **Acknowledgements**

The authors give thanks to Ana Vini for drawing the schematic view of the interaction between freshwater and marine layers. We are also grateful to the cave workers that helped us with our fieldwork: Germán Yañez, Guillermo Ruiz, Joey Pakes, Michel Vazquez, Fernando Paulin, and Amelia Weiss. This work is an outcome from projects supported by Quintana Roo Autonomous State University, the National Council of Science and Technology (CONACYT), and SEP-PRODEP.

#### **Conflict of interest**

The authors declare no conflict of interest.

*Subterranean Waters in Riviera Maya of the Yucatan Peninsula: Vulnerability... DOI: http://dx.doi.org/10.5772/intechopen.106437*


**5.8 TFE3**

Studies of the p68 promoter have shown that transcription factor E3 (TFE3) operates in a similar manner to YY1. Thus, the E Box bound by TFE3 and the E2F consensus sequence occur in close proximity in the *p68* promoter. TFE3 and E2F-3 bind to those sites cooperatively (Giangrande et al., 2003; Giangrande et al., 2004). This interaction requires E2F-3, but not TFE3 binding to DNA. Although a direct interaction between these two proteins was not be demonstrated, these two factors likely work together in a larger protein complex, or interact temporarily to recruit one another to the *p68* promoter.