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Introduction
The freshwater ecosystems in both surface and groundwater are the main sources of freshwater in the world. However, surface water represents 1.2%; ground water, 30.1%; polar ice and glaciers 68.7%. Only a small fraction of existing fresh water, almost entirely stored in aquifers (United Nations Environment Programme (UNEP, 2008). Aquifers are highly efficient interfaces with surface water through allogeneic charges, internal runoff, diffuse infiltration, recharge perched basins, and some of these structures are associated with the formation of subterranean caves (Bertelli, Dos Santos, & Bichuette, 2013).
Caves serve as collection sites for rainwater, table conditions, act as natural laboratories of biological evolution, and maintain the fauna, flora and the microbiota of unique species (Griebler & Lueders, 2009; Taylor & Holsinger, 2011; Weigand, 2013). Cave systems also have acted as a refuge for many species providing special evolutionary conditions, including regressive evolution (Villacorta, Jaume, Oromí, & Juan, 2008; Jeffery, 2009; Juan, Guzik, Jaume, & Cooper, 2010).
Worldwide there are between 10,000 and 100,000 species of obligate subterranean terrestrial species (troglobionts) and aquatic species (stygobionts). A few fishes and salamanders are included in this group but the vast majority are macroinvertebrates, especially arachnids, beetles, nematodes, mollusks, and crustaceans. These organisms have different morphological, physiological, and ethological characteristics, acquired during the historical events and adaptations to these dark and isolated environments. They are endangered, mainly by anthropogenic activities (Ubick, 2001; Culver & Sket, 2002; Tierney et al., 2015).
Mexico has over 7 000 caves of various formations and sizes that are habitats for a great diversity of species like troglobions, troglophiles, and trogloxenes contributing to biodiversity and endemism in the country, which are among the highest in the world. This is due to the physiographic, climatic, and ecological complexity of the country and a particular placement within the Nearctic and Neotropical biogeographic regions.
Therefore, the ecological conditions of both biogeographic regions overlap, resulting in the Mexican Transition Zone (MTZ), where there is a very high concentration of endemic species and biodiversity. The presence of high diversity and endemism is particularly remarkable in the region of the Pacific Southwest, considered as a Pleistocene refuge (Hoffmann, Palacios-Vargas, & Morales-Malacara 1986; Myers, Mittermeier, Mittermeier, Da Fonseca, & Ken, 2000; Hoffmann, López-Campos, & Vásquez-Rojas, 2004; Llorente-Bousquets & Ocegueda, 2008; Morrone & Márquez, 2008; Morrone, 2015).
The presence or absence of certain species in ecosystems has proven to be a very effective tool for detecting the level of disturbance, especially because of the anthropogenic activities. Some species are very tolerant of environmental change and human pollution, while others are too sensitive to these changes (Clesceri, Greenberg, & Eaton, 1999; Mafla, 2005; Bustamante, Monsalve, & García, 2008; Tione, Bedano, & Blarasin, 2011; Riley, Gerba, & Elimelech, 2011). Because of this, they have been widely used as bioindicators to determine the disturbance of ecosystems, establish protected areas, define biogeographic regions, and especially to determine water quality. Thus, some of these species are listed as protected species (Hamilton-Smith, 2001; Morrone, 2009; Corona-López, Toledo, & Morrone, 2009; De Walt et al., 2012).
Biological indicators identify at least 100 indices developed over the past ten years, of which about 60% are based on macroinvertebrates. Therefore, the suitable indices are calculated and standardized to assign values to water quality (Malard, Plenet, & Gibert, 1996; Mandaville, 2002; Mathuriau, Mercado, Lyons, & Rivera, 2012).
This report is a contribution to listings of the macroinvertebrate fauna of caves in the Neotropical Region of Mexico, and particularly to the Transition Zone. Also, represents the first study of water quality in a cave in Mexico using biotic indices.
Material and methods
Localization of Boca del Río Cave
The State of Guerrero is located within the biogeographic Neotropical Region, which spans the Caribbean, Central and South America (Figure 1, top). The municipality Chilpancingo de Los Bravos is located in the Central region of Guerrero State, and is the seat of the capital of the state that bears the same name Chilpancingo de Los Bravos (INEGI, 2010). Boca del Río Cave Apetlanca is located in the town of Acahuizotla, in the south of the State capital Chilpancingo de Los Bravos, at coordinates 17° 22’ 60” N; 99° 27’ 0” W (DMS). This cave has a length of 2576 meters and a depth of 137 meters (Figure 1).
Figure 1 Location of Boca del Río Cave. Top, a map of Mexico, dotted line indicates confluence between biogeographical regions Nearctic and Neotropical. Down, Boca del Río Cave in the State of Guerrero. Below, in rectangle, topographic map of Boca del Río Cave circles represents sampling stations (image modified from Engler, 1982).
Sampling method
Two periods of sampling were conducted in the cave Ahuizotla, from 21 to 25 February and from 11 to 14 November 2011. Three sampling sites were established: Station 1, entrance; Station 2, first steep (drop off) to 150 meters distance from the entrance; Station 3, second steep (drop off) to 320 meters from the entrance (Figure 1).
The aquatic arthropods were collected randomly with a metal landing net, the insects were taken with entomological tweezers and brushes (Barbour, Gerritsen, Snyder, & Stribling, 1999). Water temperature was 19 °C with pH ranging between 6 and 6.5 and the maximum depth in the pools was 2.5 m.
Taxonomic characterization
The macroinvertebrates were preserved in 70% alcohol, these are result of except crustacean adults that were fixed in 40% formalin, and the entire collection was transferred to the laboratory, to be identified using morphological keys (Usinger, 1956; Needham, 1981; Borror, Triplehorn, & Johnson, 1989; Westfall & May, 2006; Hanson, Springe, & Alonso, 2010; Miller & Montano, 2014).
The following indices were applied, to quantify the status of the water quality of the studied system.
The coefficient of taxonomic work (CTW)
The index enables the assessment of taxonomic collections indicating the adequate taxonomic level.
Equation (1) determines the value of CTW:
Dt |
= number of characterized families (families with the specific name). |
T |
= a total number of families (any family). |
When the CTW value is close to one this indicates appropriate taxonomic knowledge of the taxon, when it is close to zero this denotes inadequate taxonomic knowledge, because most of the collected organisms are only considered morpho-groups (Navarrete-Heredia, 2006; Naranjo López & Navarrete-Heredia, 2011).
The biological monitoring working party for Colombia (BMWP/Col)
BMWP/Col originally adapted by Armitage, Moss Wright and Furse (1983), and Alba and Sánchez (1988), and later developed for families of macroinvertebrates of the Neotropical Region in Colombia by Roldan (1999), Zamora (2007) and Vergara (2009). It is based on the level of tolerance of macroinvertebrates to pollution, using the family level as an appropriate taxon. The abscence of macroinvertebrate families that are intolerant to pollution is considered as a strong indicator of environmental biological alteration, accord to the chart of values and colors of level of water quality BMWP/Col (Table 1).
Table 1 Cartography of the water quality for the indices, BMWP, ASPT, FBI and SCI.
|
BMWP/Col (Roldan, 2003) |
ASPT/col (Arango et al., 2008) |
FBI/SV2010 (Sermeño et al., 2010) |
SCI (Saldaña et al., 2001) |
|||||
| Index value | Water quality | Index value | Water quality | Index value | Water quality | Organic contamination | Index value | Organic Pollution |
| ≥ 121 | I. Dark blue = very good | > 9-10 | Dark blue = very clean | 0.00-3.75 | 1. Dark blue = excellent | Unlikely | > 12 | Good quality |
| 101-120 | II. Clear blue = good | > 8-9 | Clear blue = unpolluted | 3.76-4.25 | 2. Clear blue = very good | Slight likely | ||
| 61-100 | III. Green = acceptable | > 6.5-8 | Green slightly = polluted | 4.26-5.00 | 3. Sky blue = good | Some likely | ||
| 36-60 | IV. Yellow = doubtful | > 3-4.5 | Yellow = moderately polluted | 5.01-5.75 | 4. Green = fair | Quite substantial is likely | ||
| 16-35 | V. Orange = critical | > 4.5-6.5 | Orange = heavily polluted | 5.76-6.50 | 5. Yellow = fairly poor | Substantial is likely | < 8 | Contaminated |
| ∞ | VI. Red = very critical | 1-3 | Red = strongly polluted | 6.51-7.25 | 6. Orange = poor | Very Substantial likely | ||
| 7.26-10.00 | 7. Red = very poor | Very substantial likely | ||||||
The family biotic index for El Salvador (FBI/SV2010)
This is an index adapted from original index FBI developed by Hilsenhoff (1988) for macroinvertebrates of the Neotropical Region of the El Salvador (Sermeño et al., 2010).
This provides an average of tolerance values for all families within the sample and allows water quality rating according to the chart for water quality to El Salvador (FBI/SV2010) (Table 1).
Average score per taxon (ASPT/Col) index
This index reflects the quality of the environment for each site using an increase in the gradient of anthropogenic impact on aquatic ecosystems described in fresh waters of the Neotropical Region in Colombia (Arango et al., 2008).
The score total for index ASPT corresponds to the level of water quality in chart of values ASPT/Col (Table 1).
Sequential Comparison Index (SCI)
This index is employed for a simple stream quality method, which is relative on estimates of differences in biological diversity by color, size, and shape. This is called the diversity index (ID). The preserved collection of fauna from a sampling station is randomized by gently shaking the collection jar. Thus, the total number of different pairs identified (“total runs”) is divided by the total number of organisms collected. This calculated number (ID) is multiplied by the numbers of different taxa (different kinds of organisms) to give the Diversity Index Total (DIT) or final SCI index (Cairns & Dickson, 1971).
The DIT value is interpreted in the chart of water quality corresponding to SCI, adapted of the original values of Cairns and Dickson (1971) by Saldaña et al. (2001) in streams in the Neotropical Region Mexico.
Clean rivers with high diversity and a balanced density generally have high index values (> 12) whereas polluted water bodies with a poor community structure generally have low index values (< 8). Intermediate values of 8 to 12 are the indication of moderately polluted waters (Saldaña et al., 2001), as shown in Table 1.
Results
Organisms collected and taxonomic characterization
A total of 29 aquatic macroinvertebrates were collected and, using taxonomic keys, were assigned to 11 families, seven genera, and four species.
The highest density and diversity were found at Station 3, with 21 macroinvertebrates belonging to seven different families. Six organisms corresponding to two families, and only two macroinvertebrates of two different families were found at Station 1.
The family Coenagrionidae was the largest, with 10 individuals collected (Table 2).
Table 2 Sampling and taxonomic characterization of macroinvertebrates found in Boca del Río Cave, in three sampling sites (station 1, 2 and 3).
| Common name | Identified family | Identified genus | Identified species | Organisms collected from sites | Identified life stages | |
| Diving beetles | Dytiscidae | Not identified | Not identified | 1 | Station 1 | 1 Aquatic adults |
| Freshwater crabs | Pseudothelphusidea | Pseudothelphusa | Not identified | 1 | Station 1 | 1 Aquatic adults |
| Spread-winged damselfliesv | Lestidae | Archilestes | Archilestes grandis | 4 | Station 2 | 2 Aquatic naiad 2 Terrestrial adults |
| Water scavenger beetles | Hydrophilidae | Not identified | Not identified | 2 | Station 2 | 2 Aquatic adults |
| Damselflies | Coenagronidae | Argia | Argia cuprea | 10 | Station 3 | 2 Aquatic naiad 8 Terrestrial adults |
| Broad-winged Damselflies | Colopterigidae | Heterina | Heterina occisa | 2 | Station 3 | 1 Aquatic naiad 1 Terrestrial naiad |
| Mayflis | Heptageniidae | Stenonema | Stenonematra | 1 | Station 3 | 1 Aquatic larva |
| Dobsonflies | Corydalidae | Not identified | Not identified | 1 | Station 3 | 1 Aquatic larva |
| Creeping water bugs | Naucoridae | Cyphocricos | Not identified | 2 | Station 3 | 2 Aquatic nymphs |
| Broad shouldered Riffle bugs | Veliidae | Ragovelia | Not identified | 2 | Station 3 | 2 Aquatic adults |
| Water striders | Gerridae | Not identified | Not identified | 3 | Station 3 | 3 Aquatic adults |
| Total | 11 | 7 | 4 | 29 | 3 | 6 |
The coefficient of taxonomic work CTW
Coefficient of taxonomic work calculated for species shows a value of 0.36, which represents a low fidelity value in the identification of species, with Argia cuprea being the most abundant species, with ten specimens.
However, the CTW indicator for the families show a value of 1.0, Coenagronidae was the most being the most abundant family.
Biologically monitoring working party (BMWP)
Based on the chart BMW/Col of assigned values of the level of tolerance of macroinvertebrates to water pollution, each family of macroinvertebrates collected from Boca del Río Cave was assigned a respective value (Table 3).
Table 3 Assignment chart for index values BMWP/Colombia to aquatic macroinvertebrates.
| Families of macroinvertebrates collected in Boca del Río Cave |
Assigned value
BMWP/Col (Roldán, 2003) |
| Heptageniidae | 10 |
| Coenagrioniidae | 7 |
| Lestidae | 8 |
| Calopterygidae | 7 |
| Dystiscidae | 9 |
| Veliidae | 8 |
| Gerridae | 8 |
| Pseudothelphusidae | 8 |
| Naucoridae | 7 |
| Corydalidae | 6 |
| Hydrophilidae | 3 |
| Total score | 81 |
The sum of assigned values for all families collected in the Cave Boca del Río is 81. According to the chart of values of level of water quality BMWP/Col (Table 1), the score of 81 corresponds to a level of water quality type III, with quality acceptable, and cartography of green color.
Sequential Comparison Index (SCI)
Results obtained from the sample of 29 macroinvertebrates identified on Cave Boca del Río are shown in Table 4.
Table 4 Obtained values of SCI index to families collected in Boca del Río Cave.
| Total number of specimens | Number of runs | Diversity index (ID) | Number different taxa |
Diversity Index
Total (IDT) ISC |
| 29 | 27 | 0.074 | 11 | 11.81 |
According to the SCI scores from the water quality (Table 1), the obtained value of 11.81 represents the water quality as moderately contaminated.
Average score per taxon (ASPT)
The index value ASPT is obtained by dividing the total score BMWP (81 points, Table 3) by the total density of families (11 families) (Table 2).
The ASPT value obtained for the aquifer Boca del Río Cave is 7.36, that corresponds to the chart of water quality, corresponding to water quality type III class, slightly contaminated (Table 1).
Family Biotic Index (FBI)
For Boca del Río Cave, this index is estimated for each smpling station, considering the number of families presents in each sampled station, the number of organisms for each family, and the total number of organisms at each station.
This index is calculated by assigning tolerance values of zero to 10 to each family. Values close to zero are assigned to the families with a higher tolerance to contamination, whereas values close to ten are assigned to the families with greater tolerance to pollution (Table 5).
Table 5 Assignment chart for index values FBI/Salvador to aquatic macroinvertebrates.
| Families of macroinvertebrates collected in Boca del Río Cave |
Assigned value
FBI/SV2010 (Sermeño et al., 2010) |
| Heptageniidae | 3 |
| Coenagrioniidae | 9 |
| Lestidae | 6 |
| Calopterygidae | 7 |
| Dystiscidae | 7 |
| Veliidae | 5 |
| Gerridae | 6 |
| Pseudothelphusidae | 6 |
| Naucoridae | 6 |
| Corydalidae | 7 |
| Hydrophilidae | 7 |
| Total score | 69 |
In the first place, it multiplies the total number of specimens of each family by its assigned value IBF/SV2010 for each family, and then the total number of individuals collected divides this value. Finally, the values obtained from all families are then added together to obtain the value of the index FBI/SV-2010 (Table 6).
Table 6 Assignment chart for index values FBI/Salvador to aquatic macroinvertebrates.
| Familie of macroinvertebrates | Abundance | Score | Abd * Sce | (Abd* Ptj)/total |
| Heptageniidae | 1 | 3 | 3 | 0.10 |
| Coenagrionidae | 10 | 9 | 90 | 3.10 |
| Lestidae | 4 | 6 | 24 | 0.83 |
| Calopterygidae | 2 | 7 | 14 | 0.48 |
| Dystiscidae | 1 | 7 | 7 | 0.24 |
| Veliidae | 2 | 5 | 10 | 0.34 |
| Gerridae | 3 | 6 | 18 | 0.62 |
| Pseudothelphusidae | 1 | 6 | 6 | 0.21 |
| Naucoridae | 2 | 6 | 12 | 0.41 |
| Corydalidae | 1 | 7 | 7 | 0.24 |
| Hydrophilidae | 2 | 7 | 14 | 0.48 |
| Total | 29 | 45 | 1 796 | 7.07 |
The obtained value FBI/SV2010 for Boca del Río Cave were 7.07, which is interpreted in the chart cartography of the water quality for the indices FBI/SV2010 (Table 1), as a decrease in water quality poor with very substantial organic pollution probable.
Discussion and conclusions
Density of identified organisms into the cave systems was low, 29 organisms macroinvertebrates, due to the restriction of nutrients that are mainly exogenous; however, the eleven families identified has given us a very clear idea of high diversity, of these organisms in this cavernous ecosystem.
Each family of identified macroinvertebrates in Boca del Río Cave has shown to be particularly tolerant to pollution (Hilsenhoff, 1988; Mandaville, 2002). Coenagrionidae, Lestidae, Veliidae, and Gerridae are associated with the natural sources of water but have tolerance to water highly polluted (Patrick & Palavage, 1994).
Dystiscidae, Hydrophilidae, Colopterigidae, Naucoridae, and Pseudothelphusoidea are families of macroinvertebrates characterized by a tolerance of water moderately contaminated (Alvarez & Villalobos, 1997).
The families Heptageniidae and Corydalidae are relatively intolerant to pollution change and are sensitive indicators of organic pollution (Borror et al., 1989; Boonsoong & Braasch, 2013).
Ten of these families of macroinvertebrates have a very wide distribution, in both Neotropical and Nearctic regions (Cumberlidge, Alvarez, & Villalobos, 2014).
The specific value, for index BMWP/Col, assigned to each family of macroinvertebrate, determined by the quality of the water in which was found the macroinvertebrates of the neotropical region of Colombia. Values close to 10 are assigned to families of macroinvertebrates intolerant to water pollution, and values close to zero are for the tolerant families to waters with some degree of contamination.
The sum of all BMW values, assigned to all the macroinvertebrates families present in a sampling, represents the final value to infer the water quality from the chart index BMWP/Col. The score of 81 corresponds to a level of water quality Type III, with quality acceptable, and cartography of green color.
The CSI index value obtained (11.81) represents the water quality as moderately contaminated, is based on the biological diversity of the families, explains the presence of the great diversity of macroinvertebrates in Boca del Río Cave. This confirms the results obtained by the index of BMW/Col, in which it is proposed that Boca del Río Cave as an environment of refuge for the different families of macroinvertebrates of the Neotropical and Nearctic region but in particular of the Transition Zone.
In the same way, that the indices BMW/Col, SCI, and the values of the index ASPT represent a level of water quality that is slightly pollute. Allowing a high variability of families in this environment.
A higher ASPT value (~10) is indicative of very clean environments that can maintain high scoring taxa while sites with low ASPT values (~0) do not support several taxa with high scores (Armitage et al., 1983). The ASPT value obtained for the aquifer Boca del Río Cave is 7.36; it represent water quality slightly contaminated.
Unlike the rate described (BMW/Col, SCI y ASPT) that indicates water quality acceptable for Boca del Río Cave, while the index of the FBI/SV2010 the water quality decreases to poor with very substantial pollution probable.
This study represents the first investigation of water quality for a cave in Mexico, especially with macroinvertebrates. There are several studies on caves but the water quality was never considered as an indicator of the health of these ecosystems, mainly due to its hidden nature and inaccesibility.
Although the methods for measuring water quality using macroinvertebrates, originally were designed for surface water ecosystems, in this study we have been able to show an overview of the state of the water quality of Boca del Río Cave, by utilizing the presence of 11 families of macroinvertebrates with different densities of organisms.
The three indices, BMWP/Col, ASPT/Col, and SCI, indicated that the water quality is slightly contaminated, which explains the high variety of macroinvertebrates families, from very intolerant (Heptageniidae and Corydalidae) to those tolerant is water highly contaminated community (Coenagrionidae, Lestidae, Veliidae and Gerridae), with predominance of the group Gerridae with 19 organisms, representing 65.5% of the sampled in the Cave Boca del Río.
These data indicate that water in Boca del Río Cave has sufficient quality to support macroinvertebrate populations. Additionally, the diversity of families and their respective densities of organisms are relatively high for the cave systems, as these systems are oligotrophic with limited sources of energy by not having primary productivity within the system.
The analysis of the water quality to region Rio Balsas, very near Boca del Río Cave, which was made by the National Council of the Water of Mexico (Conagua, for its acronym in Spanish) using both physicochemical and macroinvertebrate methods, have shown very similar results.
In the majority of the studied sites, water has good quality or has very slight contamination using both methods, physicochemical and macroinvertebrates (Conagua, 2010).
The physicochemical analysis of the water quality of the aquifer Papagayo, to which is associated the Boca del Río Cave, resulted in water of good quality, with permissible limits for human consumption (Conagua, 2013).
Water quality determined by the use of physicochemical parameters and with macroinvertebrates provide results consistent and comparable, as well as between groundwater and surface water.
On the other hand, the results of the index FBI/SV2010 showed that the level of contamination is high for all three sites, but mainly for Station 3. At this station, there is the greatest variety of families (63.63%) and the highest density of organisms (72.41%), which is probably explained by the presence of greater organic contamination in the station number 3 (that can withstand these densities of organisms). Therefore, with the depth of the cave, 320 meters at the Station 3, the conditions are changing, but still enough good conditions quality for the presence of failies with different tolerances to pollution. The high density of organisms at this station (21 organisms) was the result of the decrease of quality water and the presence of the particularly tolerant families.
Boca del Río Cave represents an important biogeographic enclave, as it is located within the Mexican Transition Zone of the region of endemism of the Sierra Madre del Sur, which is adjacent to the Basin of the Balsas, one of the main centers of greatest diversity in Mexico (Morrone, 2015). The identification of 11 families of macroinvertebrates from 29 organisms troglobites, collected in three sampling stations within, showed that no family was located in two different stations, apparently each family is very specific to an ecological niche. This may imply the existence of a complex structure between families, and the existence of a large number of micro-niches, with high potential to generate biodiversity and endemism in this ecosystem. These identified macroinvertebrates identified, with other communities of cave fauna, like bats and invertebrates, microorganisms, etc., interact with soil and walls, all associated with very fragile trophic networks. Therefore, Boca del Río Cave is an important refuge for the maintenance and generation of a variety of species.
Macroinvertebrates are an important tool, not only to monitor the quality of the water, but also for recognizing the state of these ecosystems. So it is important to study the macroinvertebrates of caves as a natural evolutionary group, because due to its high capacity of adaptation to caves, because they show very defined biogeographic patterns.
The proposal of this work is to generate the motivation to continue with the identification of species, and to differentiate the endemic groups, make sampling more extensive and intensive sampling in the entire cave and to identify possible gradients in the presence of families and species, and to associate them with niche-specificity.
It is recommended to carry out additional studies on water quality with other parameters biological and physiocochemical should be carried out on this topic, to obtain more precise data. This would allow for the development of an index specific for caves and the biogeographic regions of Mexico.
For all of the above, it is urgent to consider sustainable management of this resource in the Cave Boca del Río. This is important because it is associated to with the major source of water supply for adjacent locations and the aquifer Papagayo and to make a sustainable use of the basin for the conservation of biological diversity. Since there are organisms that have had very complex evolutionary processes, they are highly specialized and have very short tolerance limits to the environmental and anthropogenic disturbances.
