Trophic analysis of the fish community in the Ciénega Churince, Cuatro Ciénegas, Coahuila

Study area

The Cuatro Ciénegas basin is an inter-mountain closed basin. The climate is arid, with an average mean rainfall of less than 200 mm.; summer day temperatures occasionally above 44 °C and winter temperatures below 0 °C (Minckley, 1969). Despite the dry climate, the basin harbors an extensive system of springs, streams and pools.

The main source of the subterranean water is old water deposited by the end of the late-Quaternary (Meyer, 1973; Wolaver et al., 2007), which is low in levels of NaCl and carbonates, and rich in sulfates, magnesium and calcium. One of the most important characteristics of the ecosystem is its low level of phosphorus, both in the water and in the soil, in comparison to other similar environments (Elser et al., 2005). Although phosphorus is an essential nutrient in various cellular processes and is not an abundant element in the world, Cuatro Ciénegas’ phosphorus levels are below the detection level (0.3 M) (Minckley, 1969; Scanlan, Mann & Carr, 1993).

The Cuatro Ciénegas basin’s water systems are probably connected in a natural way, either underground or over the surface during the rainy season, although man-made irrigation channels have modified or interconnected most of the systems, therefore eliminating many habitats by diminishing the level of the underground water (Minckley & Cole, 1968).

The present study was done in the Churince aquatic system, which was divided into five collecting areas, considering the water level and its physico-chemical characteristics: (1) Laguna Grande o Laguna Churince, (2) Laguna Intermedia, (3) Poza Bonita, (4) Rio Churince and (5) Poza Churince (Fig. 1) (Zamudio-Valdés, 1991; Hendrickson et al., 2008). The Churince aquatic system is the oldest marsh in the Cuatro Ciénegas valley and was considered the least altered by human activity (Zamudio-Valdés, 1991). However from 2006 to 2009 a sudden 30 m decrease in the water level table was recorded. This decrease affected mainly the Laguna Grande, turning it into a desolate space full of saltpeter (Carrera, 2011).

Fish sampling

Nine samplings were carried out in the Ciénega Churince from February 2011 to May 2013 with the collection permit SAGPA/DGVS/02138, and PPF/DGOPA-140/14. Specimens were collected with a cast net of 3 × 1.5 m, 0.5 cm mesh size seine, and with dip-nets and minnow traps for jewel fish. Fish were preserved, analyzed and deposited in the Colección Nacional de Peces of the Instituto de Biología, UNAM.

Stomach content analysis

Fish stomachs were Hyslop (1980) and Laevastus (1980). Prey were documented for volumetric percentage: food volume with respect to stomach content volume; numerical percentage: the number of individuals of each food category out of the total number of individuals of all food categories in the stomach; and frequency of occurrence expressed as a percentage: the number of stomachs with one to more individuals of each food category out of all the analyzed stomachs. Data was integrated into the Index of Relative Importance (IRI) (Pinkas, Oliphant & Iverson, 1971), and the feeding coefficient, which determines the importance of food components. For the feeding coefficient, Q > 200 is considered as preferred prey, Q ≥ 20 as secondary prey and Q < 20 as rare prey. Jaccard coefficient was used to calculate the similarity of taxa ingested among fish species, in addition to estimating the overlap by means of the Piankas index. The accumulated trophic diversity (Hk) was calculated according to the method applied by Olguín, Attamedo & Beltzer (2012). Similarity of diets with respect to the identified taxa was also measured with the Jaccard index (Villareal et al., 2006)

Trophic level or position was determined in accordance to the feeding habits type of each species with respect to the Index of Relative Importance and the feeding coefficient. Trophic positions were defined as 1st level (primary producers), 2nd level (primary, secondary and tertiary) and 3rd level (decomposers) categories (Tyler, 1994).

Trophic niche amplitude quantitatively defines an organism as a generalist when it feeds on a variety of food items, and as a specialist when it preferentially eats one type of prey. The standardized Levins index was used to estimate the niche amplitude from the uniformity in the distribution of the individuals among the diverse food resources. Values of 0 to 0.60 characterize an organism as a specialist and values above 0.60 as a generalist (Krebs, 1989).

Trophic chain

The degree of similarity of the fish diets was determined using accumulative hierarchical and numerical classification analysis techniques, in order to define groups of species that share similar prey. The establishment of similar trophic groups was based on the average linkage method. A matrix was constructed using the Bray-Curtis dissimilarity index. Dendrograms were used for graphic representations.

Collected specimens

A total of 569 specimens of nine species and five families of fish were collected (Table 1). As it was not possible to identify the stomach contents of all the groups down to the lowest possible taxonomic level, these were characterized as general categories, allowing the results to be standardized, however, they are listed in annex 1 for consultation. The main qualitative characteristics of the stomach contents of the community are shown in Fig. 2, the food description of each species are as follows:

Cyprinodon atrorus Miller, 1968, cachorrito del Bolsón –Bolsón Pupfish. In the Churince aquatic system this pupfish is distributed from Laguna Intermedia to half way along the Río Churince. This species is considered threatened (NOM-59-SEMARNAT-2010). 75 specimens were analyzed (Table 1). The accumulated trophic diversity (Hk) was 3, reaching the asymptote of the curve (Fig. 3). The amplitude of the trophic niche showed a value of 0.77 (Table 1). There were 27 species as stomach items, represented in six categories. The contribution of each food category, according to the index of relative importance, was: insects 77.3, crustaceans 17.9, plants 3.25, teleosts 1.46, mites 0.18, and gastropods 0.05 (Table 2). According to the dietary coefficient, the preferred categories were crustaceans and insects (Fig. 4).

Cyprinodon bifasciatus Miller, 1968, cachorrito de Cuatro Ciénegas—Cuatro Ciénegas Pupfish. This species is restricted to thermal waters (26.7 °C–34.5 °C) in or near springs, streams and wetlands that have a constant flow of hot water and unchanging physical characteristics (Arnold, 1972). It is considered a threatened species (NOM-59-SEMARNAT-2010). 99 stomachs were reviewed (Table 1), in which 27 food items were found, within eight categories. The contribution of each food category according to IRI was: 55.18 crustaceans, 29.14 insects, 11.71 plants, 2.83 teleosts, 0.72 mites, 0.22 gastropods, 0.11 nematodes, and 0.1 spiders (Table 2). The accumulated trophic diversity (Hk) was 2.6, reaching the asymptote of the curve (Fig. 3). This species presented a value of 0.75 in the amplitude of its niche (Table 1). The feed ratio indicates that the categories of insects and crustaceans are the main food and plants are the secondary (Fig. 4).

Gambusia marshi Minckley & Craddock, 1962, guayacón de los Nadadores—Robust Gambusia. This species swims near the surface, it’s aggressive and distributed widely in the Bolsón de Cuatro Ciénegas (Miller, Minckley & Norris, 2009). The species is considered threatened (NOM-59-SEMARNAT-2010). It is the only species found throughout the whole Churince aquatic system. In order to analyze the diet, the collected specimens were divided into two groups, according to the physical and chemical characteristics of the system (e.g., temperature, plants in and outside the water, and species with which they interact in the marsh). The first group (70 specimens) was distributed from Laguna Intermedia to the middle of the Rio Churince (Table 1), the same as C. atrorus; while the second group (106 specimens) is distributed from the middle of the Rio Churince to Poza Bonita, the same as C. bifasciatus. In the first group, 32 food items in 8 categories were found. According to the IRI, they contribute as follows: insects 48.32, crustaceans 43.86, teleosts 3.98, mites 1.44, spiders 1.11, plants 0.75, nematodes 0.35, and gastropods 0.04. The feeding coefficient indicates that insect and crustacean categories are preferred (Fig. 4). The accumulated traffic diversity (Hk) yielded a value of 3, reaching the asymptote of the curve (Fig. 3). Its niche amplitude has a value of 0.86 (Table 1). In the second group were found 44 species in six categories, which according to IRI, contributed as follows: plants 39.22, insects 35.95, crustaceans 22.62, teleosts 1.00, mites 1.22, and spiders 0.67. The traffic diversity (Hk) is 2.5, reaches the asymptote of the curve (Fig. 3). The amplitude of the traffic niche is 0.95 (Table 1). The feed ratio determines that the plant and insect categories are preferential, and the crustaceans are secondary items in their diet. Jaccard’s dendrogram of both groups’ diets expressed 75% of similarity (Fig. 5).

Lepomis macrochirus Rafinesque, 1819, mojarra oreja azul—Bluegill Sunfish. This species is a bottom dweller in temperate slow-moving waters and deep, calm, stagnant areas where aquatic plants and other types of vegetation are common (Miller, Minckley & Norris, 2009). 13 specimens were analyzed, of which 18 food items were identified within 6 categories. Their contribution according to IRI was: 67.4 insects, 29.82 crustaceans, 1.33 teleosts, 1.09 nematodes, 0.13 plants, and 0.23 mites (Table 2). The feed ratio expressed that insects and crustaceous are the preferred food categories (Fig. 4). The accumulated trophic diversity is 2.8, and did not reach the asymptote of the curve (Fig. 4). The amplitude of the trophic niche has a value of 0.60 (Table 1).

Lepomis megalotis (Rafinesque, 1820), orejona roja—Longer Sunfish. This species is usually found in the higher parts of rivers and their tributaries, in standing clear or muddy waters, and in shallow water bodies. Twelve stomachs were reviewed in which 24 food items of 7 categories were found (Table 1). According to the IRI, the food categories contribute as follows: 63.05 crustaceans, 34.92 insects, 0.82 gastropods, 0.59 teleosts, 0.31 nematodes, 0.3 plants, and 0.13 spiders (Table 2). The feed ratio classifies crustaceans and insects as the main items. The accumulated trophic diversity reaches 3 without reaching the asymptote of the curve (Fig. 4). The amplitude of the trophic niche has a value of 0.75 (Table 1).

Micropterus salmoides (Lacepède, 1802), lobina negra—Largemouth Bass. This is a benthic species that tolerates a wide variety of conditions, but prefers warm, moderately clear, slow-moving or standing waters. 48 stomachs were analyzed in which 41 food items were identified and classified into five categories (Table 1). According to IRI, they contribute to the diet as follow: 56.14 insects, 40.12 crustaceans, 2.14 mites, 0.82 teleosts, 0.27 plants (Table 2). The feed coefficient classifies the crustaceans and insects as primary categories in their feeding (Fig. 4). The accumulated trophic diversity has a value of 3.2, reaching the asymptote of the curve (Fig. 3). The amplitude of the traffic niche is 0.95 (Table 1).

Herichthys minckleyi (Kornfield & Taylor, 1983), mojarra de Minckleyi—Minckley’s Cichlid. Species classified as endangered (NOM-59-SEMARNAT-2010). Minckley’s Cichlid has three morphological types, or “morphs” (Kornfield & Taylor, 1983; Minckley, 1969; Husley, Hendrickson & García de León, 2005). The main polymorphism is in the pharyngeal teeth: It is possible to find individuals with very big and strong teeth (molariform), as well as very fine, pointed and delicate teeth (papilliform). It has been documented that individuals with molariform teeth eat mainly snails, while those with papilliform teeth feed on organic matter, among other things (Minckley, 1969; Kornfield & Taylor, 1983). The piscivorous morph has more elongated head and body and its diet includes especially C. bifasciatus (Minckley, 1969; Kornfield & Taylor, 1983). Nine specimens were collected, in which 28 food items were identified and classified into eight categories. According to IRI, items contribute to the diet as follow: gastropods 54.46, plants 24.74, crustaceous 4.82, spiders 0.13, insects 7.35, teleosts 7.21, mites 0.9, and nematodes 0.52 (Table 2). The feed factor classifies gastropods as the primary category and plants and teleosts as secondary food (Fig. 4). The amplitude of the trophic niche is 0.77 (Table 1). The accumulated trophic diversity reaches 3.3 without reaching the asymptote of the curve (Fig. 3).

Hemichromis guttatus Günther, 1862, jewel fish—Jewel Cichlid. This opportunist feeder lives in the water column. Fish of this genus are bi-parental; they build nests on the bottom and care for them together. The species is native to Africa and exotic to the area (NOM-59-SEMARNAT-2010). It was first reported in March 1996 in Poza Churince (Contreras-Balderas & Ludlow, 2003). It is distributed in Poza Bonita, Río Churince and Poza Churince. A total of 102 stomachs were analyzed, in which 77 food items of seven categories were identified (Table 1). According to IRI, items contribute to the diet as follow: 43.31 insects, 35.04 crustaceous, 9.98 plants, 4.88 mites, 4.48 gastropods, 2.12 teleosts, 0.02 spiders, and 0.01 nematodes. The feed coefficient classifies insects as the primary food category and the crustaceans and plants as secondary (Fig. 4).

Cyprinella xanthicara (Minckley & Lytle, 1969), sardinita de Cuatrociénegas—Cuatrocienegas Shiner. Species classified as endangered (NOM-59-SEMARNAT-2010). This pelagic fish lives in large springs of clear water, in streams fed by springs, in areas with currents and in where there is contact between currents and standing water. It tends to concentrate above and below riffles over marl, gravel, rocks and flocculated clay. It is more abundant in the high parts of streams fed by springs, just below the source of the water (Miller, Minckley & Norris, 2009). In the Churince system, it is distributed only in Laguna Intermedia. Thirty - five stomachs were analyzed, in which 19 food items of six food categories were identified. According to IRI, items contribute to the diet as follow: 53.63 insects, 45.9 crustaceans, 0.26 mites, 0.05 plants, 0.04 gastropods, and 0.03 teleosts. The feed coefficient classifies crustaceans and insects as the main categories in the diet of this species. The accumulated trophic diversity is 2.6 without reaching the asymptote of the curve. The amplitude of the trophic niche was estimated at 0.56.Overlapping diets. The Pianka index, bold as a result; Observed Index: 0.55, Lower-tail P > 0.999 and Upper-tail P < 0.001.