Trophic ecology in an anchialine cave: A stable isotope study

Abstract

The analysis of carbon and nitrogen stable isotopes (δ13C and δ15N) has been widely used in ecology since it allows to identify the circulation of energy in a trophic network. The anchialine ecosystem is one of the less explored aquatic ecosystems in the world and stable isotope analysis represents a useful tool to identify the routes through which energy flows and to define the trophic niches of species. Sampling and data recording was conducted in one anchialine cave, Cenote Vaca Ha, near the town of Tulum, Quintana Roo, Mexico, where seven stygobitic species endemic to the anchialine caves of the Yucatan Peninsula, plus sediment, water and vegetation samples were analyzed to determine what the main nutrient sources are. We compared our results with two previous studies, one conducted in the same cave and another one from a cave in the same area, both based on the same seven species which are widely distributed in the area. Our study revealed: a) that despite a certain amount of variation in the δ13C and δ15N values of the species through time, both seasonally and interannually, the anchialine isotopic niche is much conserved; b) through contribution models we propose what are the most probable food sources for the studied species and the results confirm previous trophic classifications; and c) that the shrimp Typhlatya pearsei presents very negative δ13C values, suggesting their consumption of bacterial sources consistent with a chemosynthetic origin of organic matter. The implications of the new findings show a very stable ecosystem with the shrimp Typhlatya pearsei, as the key species to link chemosynthetic microbial production of organic matter to the anchialine trophic web.

Fig 1. Map of the Yucatan Peninsula, Mexico, with cenotes shown in blue circles, and Cenote Vaca Ha indicated by a red circle.

The map image was obtained at Natural Earth (https://www.naturalearthdata.com/) which is in the public domain. The layer with cenotes is taken from GeoComunes portal, and is in the public domain (http://132.248.14.102/layers/CapaBase:cenotes_completo2).

Fig 2. Schematic representation of Cenote Vaca Ha showing the different sections of the system, the two main water masses and the sites where water samples were taken for carbon measurements.

Fig 3. Physico-chemical profiles of the water column in Cenote Vaca Ha for the rainy and dry seasons.

(A) salinity, (B) dissolved oxygen concentration, (C) temperature, (D) pH.

Fig 4. Biplot of mean ± standard error of δ ¹³C and δ¹⁵N values for four datasets: In green the one conducted from 1993 to 1995 [11], in blue the one from 2019 [23], and rainy (black) and dry (red) seasons from this study in 2022.

Shaded areas indicate the possible food source for the anchialine fauna.

Fig 5. Bayesian mixing model results to estimate the most probable diet sources.

(A) the remipede Xibalbanus tulumensis, (B) the mysid shrimp Stygiomysis cokei, (C) the amphipod Tuluweckelia cernua, (D) the atyid shrimp Typhlatya mitchelli, (E) the atyid shrimp Typhlatya pearsei, (F) the mysid shrimp Antromysis cenotensis, (G) the isopod Creaseriella anops. Abbreviations for the probable food sources are: AC, Antromysis cenotensis; CA, Creaseriella anops; TM, Typhlatya mitchelli; POM, particulate organic matter; NB, nitrifying bacteria; MB-BP, methanotrophic bacteria, data from [30]; MB-WF, methanotrophic bacteria, data from [31].

Fig 6. Comparison of the isotopic niche of anchialine species.

(A) Bayesian standard ellipses comparing the isotopic niche of anchialine species based on four data sets [11, 23] and from the rainy and dry seasons. (B) density plots of Bayesian estimates of Standard Ellipse Areas (SEA) for the same datasets. Black dots indicate the modes of SEA, and boxed areas—Bayesian 50, 75 and 95% credible intervals; the red “x” indicates the mean.