Research Article |
Corresponding author: Sergio Benítez ( sergioska99@hotmail.com ) Academic editor: Oana Teodora Moldovan
© 2019 Sergio Benítez, Thomas M. Illife, Benjamín Quiroz-Martínez, Fernando Alvarez.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Benítez S, Illife TM, Quiroz-Martínez B, Alvarez F (2019) How is the anchialine fauna distributed within a cave? A study of the Ox Bel Ha System, Yucatan Peninsula, Mexico. Subterranean Biology 31: 15-28. https://doi.org/10.3897/subtbiol.31.34347
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A study describing the diversity and distribution pattern of the stygobitic fauna in the Ox Bel Ha anchialine cave system adjacent to the Caribbean coast of the Yucatan Peninsula, Mexico is presented. A total of 15 species of crustaceans were collected in three surveys at four points situated along a 10.2 km transect perpendicular to the coast line. A freshwater mass dominated throughout the transect with a halocline that appeared progressively deeper, from 10 to 18 m, with increasing distance from the coast. All the recorded species, except for one, occurred throughout the transect with no defined pattern. Abundance and species richness did not vary significantly with distance from the coast, whereas diversity (H’) peaked in the second sampling site at 3.17 km from the coast. As expected, most of the organisms occurred only in the freshwater layer, except for the remipede Xibalbanus tulumensis (Yager, 1987) that was found always at or below the halocline, and five other species that were found above and below the halocline. In the horizontal scale, species composition and occurrence mixed without a defined pattern, both, for sampling dates and sites. The results show that the analyzed fauna is distributed throughout the 10.2 km transect without showing any defined horizontal zonation pointing to a high connectivity among all sections. Due to the high connectivity within the caves in the area, it is expected that significant variation in species composition and distribution will be found at a larger regional scale.
Diversity, abundance, vertical distribution, connectivity
The anchialine cave systems of the world have been intensely studied during the last three decades since their discovery and the improvement of diving techniques to explore them (
The anchialine caves of the Yucatan Peninsula (YP) along the Caribbean coast of Mexico between the City of Cancun and the town of Tulum (Fig.
While several studies have explored the distribution of anchialine fauna at a regional scale (
The anchialine caves of the YP are unique in terms of their extension and in the relative ease with which they can be accessed through cenotes. Although the explorations made by divers suggest that there is a high connectivity throughout most of the caves’ passageways, no studies have been conducted to describe if the anchialine fauna is distributed uniformly within large caves or if there is a zonation or differential occupation of defined habitats or sections. In this study we analyzed the spatio-temporal variation of the anchialine fauna along a 10.2 km transect (distance on the surface) in the Ox Bel Ha (OBH) anchialine cave, one of the largest underwater caves on earth (
A transect was established along the northern branch of the OBH system, south of the town of Tulum, Quintana Roo, Mexico (Fig.
Three surveys were conducted in February, August and December, 2013. A group of three divers performed several tasks in each survey. First, one diver profiled the water column for temperature, salinity, dissolved oxygen concentration, pH and conductivity with a Hydrolab DataSonde 5X probe in the area where the biological sampling was going to be conducted; a second diver obtained samples from the water column above and below the halocline with two separate plankton nets with a 500 µm mesh; and the third diver captured individual organisms with glass vials recording the depth at which the sample was taken.
All samplings, in the four cenotes and adjacent cave in the three sampling dates, were conducted by three divers who performed the same tasks. The divers followed the same route inside the caves in every survey. Air supply was the same for all dives which lasted between 90 and 100 min, so that sampling effort was as similar among surveys as possible. Although neither fish nor copepods were considered in our sampling, the endemic blind brotula, Typhliasina pearsei (Hubbs, 1938), was observed in all four cenotes. All specimens were collected under the scientific collector’s license issued to FA (FAUT 0104) by the Mexican environmental authority (SEMARNAT).
All samples were preserved in 80% EtOH and all organisms identified to species. Appropriate taxonomic keys were used to identify the collected organisms: amphipods (
To test for differences in the distribution of organisms along the transect abundance data were tested for normality with a Kolmogorov-Smirnov test, and a Cochrane test of homocedasticity. One-way analysis of variance was used to compare abundances by site and by sampling date. In order to describe the number of species and their abundances Shannon’s diversity index was obtained by site (
Relationships among the faunal assemblages of each cenote were examined via a similarity matrix constructed using the Jaccard’s coefficient. Jaccard’s similarity is, in this framework, a measure of the degree of overlap between sample points in terms of species occurrence and composition. The resulting similarity matrix was used for both cluster analysis (UPGMA) and non-metric multidimensional scaling (nMDS), as has been suggested by several authors (
In cenote Tábano salinity ranged from 2 to 32 psu, with a halocline present at a depth of 11–12 m; for cenote Odyssey the values were: 0.6 to 35 psu and a halocline between 13–14 m; for cenote Muknal 0.5 to 33 psu, and a halocline between 14–15 m; and for cenote Bang 1 to 34.5 psu, and a halocline at 18–20 m depth (Fig.
Water quality parameters recorded in the three samplings (February, August and December, 2013) in the four sites of the Ox Bel Ha system, Quintana Roo, Mexico: Tábano, Odyssey, Muknal, Bang. Columns correspond to: depth of the halocline in m, salinity in psu, temperature (°C), pH and dissolved oxygen concentration in mg/l ([O2]). Dashes indicate readings not taken, “NR” stands for not recorded when the halocline was deeper than the deepest surveyed area.
Salinity | Temperature | pH | [O2] | ||||||
Halocline | Above Halocline | Below Halocline | Above Halocline | Below Halocline | Above Halocline | Below Halocline | Above Halocline | Below Halocline | |
February | |||||||||
Tabano | 10–12 | 4.34 | 30.4 | 26.9 | 27.2 | 6.9 | 7.1 | – | – |
Odyssey | 12–13 | 4 | 32.1 | 25.7 | 26.7 | 6.8 | 7.3 | – | – |
Muknal | 13 | – | – | – | – | – | – | – | – |
Bang | 18–19 | 2.2 | 32.7 | 25.5 | 25.8 | 6.9 | 7.4 | – | – |
August | |||||||||
Tabano | 10–11.7 | 4.34 | 27.9 | 26.1 | 26.4 | 7.7 | 7.8 | 0.21 | 0.32 |
Odyssey | 12–12.5 | 5.1 | 33 | 25.8 | 26.7 | 7.7 | 7.8 | 0.38 | 1.5 |
Muknal | 15–16.5 | 2.99 | 33 | 25.6 | 26.3 | 7.6 | 7.9 | 0.78 | 1.95 |
Bang | 18–20.9 | 2.2 | 32.8 | 25.5 | 25.8 | 7.7 | 7.8 | 0.69 | 2.1 |
December | |||||||||
Tabano | 12 | 4 | NR | 26 | NR | 6.72 | NR | 5.6 | NR |
Odyssey | 13–14 | 4.9 | 31.9 | 25.6 | 26.4 | 6.7 | 6.9 | 0.44 | 2.42 |
Muknal | 16–18 | 4.3 | 31.5 | 25.8 | 26.2 | 6.7 | 6.9 | 0.31 | 2.1 |
Bang | 18–20 | 2.71 | 26.9 | 25.8 | NR | 6.5 | NR | 0.15 | NR |
A total of 368 organisms were collected, 123 in cenote Tábano, 93 in Odyssey, 88 in Muknal, and 64 in Bang. Although total abundance decreases with increasing distance from the coast, mean abundance did not differ significantly along the transect (Anova, F[3, 11] = 0.8763, p = 0.5039; Fig.
The distribution of species within the transect showed a slight variation, cenote Tábano had a total of 9 species, Odyssey 12, and Muknal and Bang 11; the mean species richness found did not differ among cenotes (Anova, F[3, 11] = 0.25, p = 0.8587; Fig.
Occurrence of species by site (Tábano, Odyssey, Muknal, Bang) and sampling (F = February, A = August, D = December) in the Ox Bel Ha system, Quintana Roo, Mexico. In blue species that occurred in the four sites, in green species that occurred in three of the four sites, in yellow species that occurred in two of the four sites and in red the single species that occurred in just one site.
Tabano | Odyssey | Muknal | Bang | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
F | A | D | F | A | D | F | A | D | F | A | D | |
Typhlatya mitchelli | ● | ● | ● | ● | ● | ● | ● | ● | ● | ● | ● | ● |
Tulumella unidens | ● | ● | ● | ● | ● | ● | ● | ● | ● | ● | ● | |
Tuluweckelia cernua | ● | ● | ● | ● | ● | ● | ● | |||||
Creaseriella anops | ● | ● | ● | ● | ● | ● | ● | ● | ||||
Creaseria morleyi | ● | ● | ● | ● | ● | ● | ● | |||||
Typhlatya dzilamensis | ● | ● | ● | ● | ● | ● | ● | |||||
Typhlatya pearsei | ● | ● | ● | ● | ● | ● | ||||||
Stygiomysis holthuisi | ● | ● | ● | ● | ||||||||
Xibalbanus tulumensis | ● | ● | ● | |||||||||
Mayaweckelia cenoticola | ● | ● | ● | |||||||||
Antromysis cenotensis | ● | ● | ● | ● | ||||||||
Humphreysella mexicana | ● | ● | ● | |||||||||
Stygiomysis cokei | ● | ● | ● | |||||||||
Metacirolana mayana | ● | ● | ● | |||||||||
Calliasmata nohochi | ● |
Shannon’s diversity index (H) varied from 1.765 in Tabano to 2.195 in Odyssey, with Muknal and Bang having intermediate values (Fig.
The analysis of similarity shows three groups in which all four cenotes and the three surveys are mixed (Fig.
Results of the multivariate analysis of variance (“Adonis” routine in the statistical software package R 3.1.3;
Df | Sums. Of Sqs. | Mean. Sqs. | F. Model | R2 | Pr(>F) | |
DC | 1 | 0.34744 | 0.34744 | 1.48583 | 0.13756 | 0.2079 |
pH | 1 | 0.37364 | 0.37364 | 1.59785 | 0.14793 | 0.1089 |
Halocline | 1 | 0.32141 | 0.32141 | 1.37451 | 0.12726 | 0.2772 |
DC: pH | 1 | 0.12133 | 0.12133 | 0.51888 | 0.04804 | 0.8218 |
DC: Halocline | 1 | 0.23741 | 0.23741 | 1.01526 | 0.094 | 0.4356 |
pH: Halocline | 1 | 0.11867 | 0.11867 | 0.50748 | 0.04698 | 0.8416 |
DC: pH:Halocline | 1 | 0.07044 | 0.07044 | 0.30125 | 0.02789 | 0.9604 |
Residuals | 4 | 0.93535 | 0.23384 | 0.37033 | ||
Total | 11 | 2.52568 | 1 |
The obtained results on the distribution and abundance of anchialine fauna along a 10.2 km transect in the OBH cave, suggest the existence of a high connectivity throughout the conduits that prevent a horizontal zonation. The hydrology of this area along the Caribbean coast of the YP has been studied showing the presence of a dynamic “subterranean estuary” where saline water penetrates inland below a freshwater lens and where groundwater discharge can be considerably high (
The hydrological connectivity amongst caves within the anchialine system in this area of the YP allows species to distribute throughout the conduits without a defined pattern. Our results show that most of the recorded species can occur in any section of the studied cave system. The limitation for the species that are restricted to the high salinity water mass, such as the remipede X. tulumensis, in this particular branch of the OBH would be the absence of a marine layer due to the shallow conduits. The conduits develop at a depth of 12 to 14 m, but with an irregular bathymetry large sections of cave could be above the level of the halocline. In contrast, the freshwater species can exlpoit a much larger area.
The number of anchialine species recorded in this study (15) represents about 27% of the known diversity for the anchialine caves of the YP (
While species composition along the transect did not show any defined pattern, abundance of organisms shows a slight, not significant, trend to decrease with increasing distance from the coast. The amount of nutrients could be increasing towards the coast where organic matter that enters via cenotes or percolation from the rainforest floor accumulates due to the circulation of freshwater (
The obtained results suggest that isolation within a cave along the Caribbean coast of the YP would not be significant to allow for population differentiation. The high degree of connectivity represents a continuum, at least in the freshwater/brackish water layer above the halocline, allowing for free movement of organisms. Thus, the scale of variation among populations that would be expected would correspond to a regional scale throughout the YP. In fact, several species endemic to this part of the YP (such as the remipede Xibalbanus tulumensis, and the amphipod Tuluweckelia cernua) are common in the whole Caribbean cave area that runs from Puerto Morelos to Tulum, in the state Quintana Roo.
The sampling along the transect in the OBH cave shows that the anchialine fauna is distributed throughout the flooded cave without a defined pattern. The hydrological data obtained is consistent with a high connectivity system typical of the cavernous area in this part of the Caribbean coast of Mexico. As expected most of the anchialine fauna found are freshwater species, with only a few restricted to the high salinity water mass.
The first author gratefully acknowledges the Posgrado en Ciencias del Mar y Limnología, UNAM, for providing the means to conduct this study and the financial support through aCONACYT scholarship. We are indebted to José Luis Villalobos, Olinka Cortés, Brenda Durán, Arturo Mora, Bil Phillips, David Brankovits, Tyler Winkler and Brett Gonzalez for their help in the field, diving and processing samples and data. Field work was conducted with funding from two (2014, 2018) Texas A&M – CONACYT Collaborative Research Grants awarded to T.M. Iliffe and F. Alvarez. Funding from DGAPA-PAPIIT-UNAM grant IN208519 and CONACYT grant 155644 awarded to F. Alvarez are also acknowledged.