Habitat use by the "Escamolera" ant (Liometopum apiculatum Mayr) in central Mexico

Uso de hábitat por la hormiga escamolera (Liometopum apiculatum Mayr) en el centro de México

J. D. Cruz-Labana¹, L. A. Tarango-Arámbula²*, J. L. Alcántara-Carbajal¹, J. Pimentel-López², S. Ugalde-Lezama³, G. Ramírez-Valverde⁴, S. J. Méndez-Gallegos²

¹ Ganadería, Campus Montecillo. Colegio de Postgraduados. 56230. Montecillo, Estado de Mexico.

³ Suelos. Universidad Autónoma Chapingo. 56230. Chapingo, Estado de México.

⁴ Estadística. Campus Montecillo. Colegio de Postgraduados. 56230. Montecillo, Estado de Mexico.

Received: January, 2014.
Approved: July, 2014.

Abstract

In rural areas of Mexico, the native "escamolera" ant (Liometopum apiculatum Mayr) is socioeconomically important. However, this ant is being exploited unsustainably, and studies of habitat of this species in central Mexico are nonexistent. During spring-summer 2012, fourteen habitat variables were evaluated, habitat use by the ant was identified and its nest density was estimated. Data were analyzed with stepwise logistic regression, correspondence analysis, Chi-square and simultaneous Bonferroni confidence intervals analyses, and the minimum Akaike Information Criteria. The variables that better described the presence of the ant were width of the agave pineapple, percentage of agaves infested with scale insects, woody plant-cacti-agave density, soil cover and terrain slope. The probability of finding nests increased (odds ratio> 1) when the width of the agave pineapple and the percentage of agaves with scale insects increased. In contrast, the probability decreased (odds ratio< 1) when the slope of the terrain and bare soil increased. The ant selected (p≤0.05) flat terrain (0-10 % slope) and southwest-facing slopes, but avoided microphyllous shrub habitats, moderately flat terrain (1-20 % slope), southeast-facing slopes and terrain of the lowest available elevation (1940-2050 m). Soil cover at nests sites was composed of grasses (27.5 %), bare soil (24.5 %), rock (20.2 %), herbs (20.2 %) and shrubs (7.6 %). The nest density was higher (α=0.05) in the moderate level of disturbance (11.9 nests ha^-1). The ant did not use habitat components according to their availability, avoided bare soil, land with low elevation and selected the slopes with southwest exposure.

Key words: Liometopum apiculatum Mayr, agave, arid areas, insects use, management.

Resumen

En las zonas rurales de México, la hormiga nativa "escamolera" (Liometopun apiculatum Mayr) tiene importancia socioeconómica. Sin embargo, esta hormiga es explotada de manera no sustentable y no existen estudios del hábitat de esta especie en el centro de México. Durante la primavera verano de 2012, se evaluaron catorce variables del hábitat, se identificó el uso del hábitat por la hormiga y se estimó su densidad de nidos. Los datos se analizaron con regresión logística por pasos (stepwise), análisis de correspondencia, Ji cuadrada y análisis simultáneos de intervalos de confianza Bonferroni, así como el Criterio de Información Akaike mínimo. Las variables que describen mejor la presencia de la hormiga fueron ancho de la piña del agave, porcentaje de agaves infestados con insectos escama, densidad de plantas leñosas-cactus-agaves, cobertura del suelo y pendiente del terreno. La probabilidad de encontrar nidos se incrementó (tasa de probabilidad > 1) cuando aumentaron el ancho de la piña del agave y el porcentaje de agaves con insectos escama. En contraste, la probabilidad disminuyó (relación de probabilidad < 1) cuando la pendiente del terreno y el suelo desnudo aumentaron. Las hormigas seleccionaron (p≤0.05) terrenos planos (0-10 % de pendiente) y pendientes hacia el suroeste, pero evitaron los hábitats de matorral micrófilo, terrenos moderadamente planos (1-20 % de pendiente), pendientes hacia el sureste y terrenos con la menor elevación disponible (1940-2050 m). La cobertura de suelo en los sitios de nido estuvo compuesta de pastos (27.5 %), suelo desnudo (24.5 %), roca (20.2 %), hierbas (20.2 %) y matorrales (7.6 %). La densidad de nidos fue mayor (α=0.05) en el nivel moderado de perturbación (11.9 nidos ha^-1). Las hormigas no usaron los componentes del hábitat con base en su disponibilidad, evitaron el suelo desnudo y los terrenos con baja elevación, y eligieron las pendientes con exposición hacia el suroeste.

Palabras clave: Liometopum apiculatum Mayr, agave, zonas áridas, uso de insectos, manejo.

INTRODUCTION

Arid and semi-arid regions contain valuable natural resources that, if well managed, may derive in diverse long-term economic benefits. Ants are important components of these regions, they constitute a significant portion of the animal biomass and act as ecosystem engineers (Folgarait, 1998). Ants are able to modify environmental conditions to create appropriate microhabitats (Hithford et al., 2008) by increasing fertility and quality of the soil (Amador and Gorres, 2007). Moreover, they can be used as indicators of ecosystem changes and for rehabilitating logging and grazing areas (Andersen and Majer, 2004).

An economic, ecological and nutritionally important species in semiarid areas of southern Chihuahuan Desert in South-Central Mexico, is the escamolera ant (Liometopum apiculatum Mayr) (Velasco et al., 2007; Ambrosio-Arzate et al., 2010). Its larvae, known as escamoles (immature stages of the reproductive caste) (Hoey-Chamberlain et al., 2013), are extracted from nests at the beginning of the spring and sold for human consumption. The word "escamol" derives from the Nahuatl language word "azcatmolli" which means ant (=azcatl) stew (molli) (Ramos et al., 2013). Escamoles are considered a delicacy and regional prices range between US $ 40 and US $ 50 kg^-1. Ramos-Elorduy et al. (2006) indicate that the price can reach up to US $ 200 dollars. Escamoles have a protein content of 39.7 mg 100 g^-1 (Ramos-Elorduy and Pino, 2001).

Escamoles are a viable resource in arid regions because its extraction does not require any economic input and they have an extensive distribution. This species ranges from Southwestern United States and northwestern to southeastern Mexico where, it is found in fifteen states from Chihuahua to Quintana Roo (Del Toro et al., 2009). In Mexico, the escamolera ant is exploited in the states of Michoacan, Colima, Chihuahua, Durango, Hidalgo, Queretaro and the Distrito Federal (Del Toro et al., 2009).

However, economically important native insects such as the escamolera ant, the agave red worm (Comadia redtenbacheri Hamm) and the agave white worm (Acentrocneme hesperiaris W.) are exploited unsustainably (De Luna-Valadez et al., 2013).

Habitat fragmentation of the soil biota and its effects on the density of the micro-invertebrates are poorly documented (Chust et al., 2003a, b). In Mexico, there is only one study that addresses the association of the escamolera ant with the agave in the state of Zacatecas (Esparza-Frausto et al., 2008), but fundamental aspects of its biology and ecology are still unknown.

Given the importance of insects as components of desert ecosystems (Hithford et al., 2008), and in particular the use of the escamolera ant larvae and the economic benefits for the Mexican rural sector, it is indispensable to determine ant habitat components. Therefore, the objectives of this study were: 1) to identify the habitat components that better explain the presence of the ant in the ejido Pocitos, municipality of Charcas, San Luis Potosi; 2) to determine whether ant uses vegetation types, slope, elevation and aspect, according to their availability; and 3) to estimate the density of ant nests (Liometopum apiculatum Mayr) in areas representatives of three levels of ecosystem disturbance.

MATERIALS AND METHODS

Description of the study area

The study area is located in the southern region of the Chihuahuan Desert (Giménez and González, 2011). This research was conducted during spring and summer 2012 in the ejido Pocitos, municipality of Charcas, San Luis Potosi. This ejido (a Mexican system of cooperative land tenure) is located 22 km northeast of the town of Charcas, between 23° 06' 32" and 23° 13' 04" N and 100° 54' 03 "and 101° 01' 02" W, at an elevation between 1979 and 2505 m and covers an area of 6422 ha.

The climate in the area is semidry temperate BS₀kw (x') with rainfall occurring from June to September. Average annual temperature and precipitation range from 12-18 °C and 300-400 mm, respectively. Main vegetation types are microphyllous, crassicaule (cacti) and rosette-like shrubland (Rzedowski, 1965; 1978), and zacatal (tall grasses). In the higher elevations of the ejido there are oak forests (Quercus hintoniorum, Q. greggii, Q. mexicana, Q. pringlei and Q. laeta) (Giménez and González, 2011), and open areas with scattered junipers (Juniperus spp.) (González et al., 2007).

Ant presence and habitat use

The quantified variables and methods of their assessment are described in Table 1. Also, woody plants and cacti (Opuntia spp.) (ant foraging substrates), mesquite (Prosopis spp.), yuccas (Yucca carnerosana and Y. filifera), acacias (Acacia spp.), junipers (Juniperus spp.) and agaves infested with scale insects (Hemiptera), were counted within the plots to estimate their density and percentage of infestation.

To determine the habitat components that most explain the presence of the ant, a stepwise logistic regression model was used (p≤0.05) with JMP 7.0 software (SAS Institute, 2007; Guisan and Zimmermann, 2000; Dos Santos and Mora, 2007) as well as an analysis of correspondence.

Chi-square analysis was used to determine if vegetation type, categories of slope, aspect and elevation were selected (i.e., used more in proportion to availability), or avoided (i.e., used less than proportion to availability) by the ant. To assess habitat use, for the entire study area, the availability (size of the area in ha) of each of the categories of those habitat variables (Table 2) were quantified using Arc Map 9.3 and topographic maps at a scale of 1:50000 (SAGARPA, 2012). If a statistical difference (p≤0.05) was detected between use (number of nests in each category) and availability (size of the area) of these components (Neu et al., 1974), simultaneous Bonferroni confidence intervals were used to determine habitat preferences (Byers et al., 1984).

Density of ant nests

Insects has been considered bioindicators of anthropogenic disturbance, they have been recognized as important indicators of ecosystem quality due to their rapid response to environmental variability (Otavo et al., 2013). The density of ant nests was estimated at three levels of ecosystem disturbance within the study area: A (slightly disturbed), B (moderately disturbed) and C (highly disturbed).

The A category encompassed an area grazed by cattle and goats; this site presented between 15 and 20 % of bare soil. The most common plant species were junipers (Juniperus spp.), agave (Agave salmiana), prickly pear (Opuntia spp.) biznaga (Echinocactus platyacanthus), yuccas (Yucca filifera and Y. carnerosana), mesquite (Prosopis spp.), acacias (Acacia spp.), and grasses, among others (Figure 1A).

The B category was characterized by the presence of lechugilla (Agave lechuguilla), relict juniper and agaves; this area was intensively grazed, eroded and percentage of bare soil was between 20 and 30 % (Figure 1B). The level C area with moderate grazing, had poor vegetation cover (bare soil percentage above 30 %) compared with the levels A and B, and was characterized by the presence of yuccas (Yucca carnerosana, Y filifera) and sparsely scattered native agaves (Figure 1C).

Nest density was estimated using 200-m-long and 100-m-wide transects (50 m to the left and 50 m to the right of the center line; 20000 m²). Three transects were randomly distributed in each level of disturbance. The perpendicular distances from nests to the centerline of transects were measured and recorded. The density of nests was estimated with the Distance 6.0 program selecting the best model with minimum Akaike Information Criteria (Buckland et al., 1993).

RESULTS AND DISCUSSION

The variables that better explained (p≤0.05) the presence of ant nests were the width of the agave stalk, number of agaves with scale insects, woody plants-cacti-agave density, ground cover (bare soil) and slope (Table 3). The probability of finding ant nests in the study area increased according to the value of odds ratio (> 1) of the habitat variable. Thus, the odds of finding ant nests in the study area increased with the presence of greater agave stalks, at sites with a higher component of agaves with scales and at areas with greater density of woody plants, cacti and agave. In contrast, the probability of finding ant nests decreased with increments in slope of the terrain and bare soil (Table 3).

The logistic regression analysis identified density of woody plants and cacti as an important component (odds ratio = 1.005). More specifically the correspondence analysis identified that the presence of mesquites, yuccas, acacias and agaves infested with scale insects explain the occurrence of the escamolera ant in the study area (Figure 2, Table 4, 5).

The ant did not use the habitat components according to their availability. There were significant differences in the observed and expected frequencies for the variables vegetation type, slope of the terrain, aspect and elevation (Table 6). The Bonferroni confidence intervals (Byers et al., 1984) indicated that the ant showed a preference for (p≤0.05) flat terrain and southwest-facing slopes. By contrast, it tended to avoid (p≤0.05) microphyllous shrub land, moderately flat terrain, southeast-facing slopes, and very low terrain (Table 6). The other habitat components (rosetophillous and crasicaule shrub land; middle and steep slope; northeast and northwest aspect and low, middle and high elevation) were used according to their availability (p≤ 0.05). The average soil cover at nesting sites were grasses (27.5 %), bare soil (24.5 %), rock (20.2 %), herbs (20.2 %) and shrub (7.6 %).

The density of nests in the disturbance level A was 6.8 nests ha^-1, 11.9 nests ha^-1 at level B and 1.19 nests ha^-1 level C. The overall average nest density for the study site was 6.06 ant nests ha^-1 (α=0.05).

Specifically, there was a significant association of the ant with increasing agave densities and stalk widths (1298 agaves vs. 433 agaves ha^-1 at used and unused sites, respectively). This plant is commonly used by the ants for nesting (49 of 54 nests recorded in this study were associated with the agave). Ant nests are commonly found at the base of the agave at a depth that ranges from 15 to 120 cm), most likely because agaves function as thermal cover and foraging areas (e.g., the ant foraging trails are often spread among the agaves). The ant probably seeks agaves infested with scale insects (Acutaspis sp) because they feed on their secretions (trophobiosis) throughout the year (Velasco, 2007). We found that 61 % of the agaves around the nests were infested with scale insects. The association of escamoles with agaves is common (Mora-López et al., 2011).

Liometopum apiculatum M. is omnivorous (Hoey-Chamberlain et al., 2013). Velasco et al. (2007) reported that ant consume insect pupae, crustaceans, annelids, mollusks, dead vertebrates, animal droppings and floral nectar of Opuntia spp., common species in the study area. In this regard, Miller (2007) notes that the ant has a mutualistic association with cardenche (Opuntia imbricata; imbricate prickly pear), and aggressively defends the plant from herbivores and seed predators. Ants are an important component of arid ecosystems and constitute a significant portion of the animal biomass, acting as ecosystem engineers (Jones et al, 1994; Folgarait, 1998 López-Riquelme and Ramón, 2010), they are able to modify environmental conditions to create suitable microhabitats (Hithford et al., 2008), increase fertility and soil quality, and control arthropod populations (Amador and Görres, 2007; López-Riquelme and Ramón, 2010). They can also be indicators of ecosystem changes and used to rehabilitate logging and grazing areas (Andersen and Majer, 2004).

The logistic regression analysis identified the width of the agave and higher plants to be important components of the habitat of the ant (Table 3). Similarly, the correspondence analysis indicated that agave, agave-scaled insect, agave-width as well as higher plants (opuntia, mesquite, yucca, acacia and juniper) contributed with 48.31% of the variation (Figure 2, Table 4, 5). More specifically, the plants that more contributed to this variation were mesquite, yucca and juniper (Table 4). These plants offer the escamolera ant, as well as other ant species, vegetation conditions, structure and protection for their foraging activities (Wisdom and Whitford, 1981; Bestelmeyer and Schooley, 1999; Retana and Cerdá, 2000). Also, the vegetation structure can influence the distribution of insect food for Liometopum apiculatum Mayr and selection of nesting sites (Johnson, 2000; Hoey-Chamberleyn et al., 2013).

In this study, ant preferred southwest-facing slopes as nest sites as did ants reported by Ramos-Elorduy et al. (1986) in Michoacan, Mexico. This study differs from those reported by Eastlake and Chew (1980), who found that in Arizona, escamolera ants preferred north and west-facing slopes to nest. However, it is possible that southwest-facing slopes in central Mexico provide better environmental conditions (temperature and atmospheric humidity) for nesting.

In addition, the ant avoided very low elevation habitats (1940-2050 masl). This behavior is possibly due to agricultural activities, which occur at lower elevations. Also the surrounding areas are dominated by creosote (Larrea tridentata (D.C.) Cobille), a plant species poorly associated with the ant. Castro et al. (2008), in a study of ants in Peru, also emphasized that the species decreases with elevation.

The significant association of the escamolera ant in central Mexico with the agave (Agave salmiana Otto Ex Salm ssp. crassispina (Trel) Gentry) indicates that efforts to conserve and manage this insect should focus on sustainably managing this habitat. However, management is complicated because local farmers use maguey plants for other commercial uses such as mezcal manufacture (García-Herrera et al., 2010; Martínez et al., 2012), forage production, and for white and red worm production and extraction (Esparza-Frausto et al., 2008; García-Herrera et al., 2010). Their management is further complicated because of mismanaged rangelands, the use of acacias and mesquites as firewood, while recurrent droughts in recent years in the center of Mexico aggravate these problems (Galindo and García, 1986; Ruiz and Febles, 2004; Andrade et al., 2009).

The probability of finding the escamolera ant decreased with increasing bare soil. However, the ant in the study area occurs under poor vegetation cover conditions (the amount of coverage of bare soil and rock was 44.7 %) resulting from overgrazing (Herrera et al., 2011). Consequently, these habitat conditions have a negative effect on the production of escamoles. In the study area, there was an average production of 0.185±0.137 kg per nest (n=54 nests) during the first harvest of 2012. This was less than that reported for San Juan Teotihuacan, state of Mexico (Ambrozio-Arzate et al., 2010), which depending on habitat conditions, the production varied from 0.4 to 0.8 kg/nest. In addition, Ramos-Elorduy and Levieux (1992) reported that the ant may produce between 3-3.6 kg of escamoles, while in Michoacan the ant produces 3.0 kg per nest in the first harvest and between 1.5-2 kg in the second (Ramos-Elorduy et al., 1986).

The ground cover is an important habitat component for the ant, especially where it requires protection from high temperatures. Therefore, the coverage offered by grasses, herbaceous plants, shrubs, woody plants and cacti is important for the species. Although the proportion of bare soil and rock was high (44.7 %), it is likely that the ants in the study area can survive with poor soil coverage conditions due to its ability to build galleries (Ramos-Elorduy et al., 1986) and tunnels (Espinoza and Santamarina, 2010). Also during the day, while foraging, they are able to move underneath woody debris present on the surface of the soil. In addition, the species is diurnal and nocturnal. Shapley (1920) and Espinoza and Santamarina (2010) reported that ants show special excavation and transport strategies since they use their antennas to evaluate the mobility of soil particles, remove particles with mandibles and legs, transport them and return to the tunnel face.

In this study, the ant uses habitat components differentially, showing higher occurrence in certain combinations of them. Also, we recorded the highest ant-nest densities at the disturbance levels B and A with an overall average of 6.06 nests ha^-1. In San Juan Teotihuacan, depending on habitat conditions, the density of ant nests ranged from 8 to 10 nests ha^-1 (Ambrosio-Arzate et al., 2010).

CONCLUSIONS

There was a very noticeable association between the presence of Liometopum apiculatum Mayr and agaves (Agave salmiana Otto Ex Salm ssp. crassispina (Trel) Gentry), and density ofwoody plants and cacti. The ant did not use habitat components according to their availability, avoided bare soil, land with low elevation and selected the slopes with southwest exposure. Nest density was higher in the ecosystem moderately (B) and slightly disturbed (A). Escamolera ant larvae can be an economically viable resource, but are being extracted unsustainably. Major challenges include habitat loss, degradation and fragmentation as a result of mismanaged landscapes. Rural extension education programs need to be instituted to develop management schemes to ensure the sustainable use of this species. The results obtained in this research are a baseline for future research and management of the species in the central region of Mexico and their sustainable use by rural communities.

ACKNOWLEDGEMENTS

We thank collectors of "escamoles" of the ejido Pocitos, Charcas San Luis Potosí, for giving us permission for the study, and supporting the field work.

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