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Mastozoología neotropical

versão impressa ISSN 0327-9383versão On-line ISSN 1666-0536

Mastozool. neotrop. vol.26 no.1 Mendoza jun. 2019

 

NOTA

Record of a population and description of some aspects of the life history of Notocitellus adocetus in the north of the state of Guerrero, Mexico

 

Daniel Flores-Alta, Francisco A. Rivera-Ortíz and Ana M. Contreras-González

Unidad de Biotecnología y Prototipos, Laboratorio de Ecología, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Los Reyes Iztacala. Tlalnepantla, Estado de México, México [correspondencia: Ana M. Contreras-González <amcontrerasg@comunidad.unam.mx>].


ABSTRACT

The rodent Notocitellus adocetus is endemic to Mexico, and little is known about its life history. We describe a population of N. adocetus living in the north of the state of Guerrero and provide information about its biology. Measurements were made from June 2015 to October 2017. The species was active throughout the day in corn crops, but not in tropical deciduous forest. Notocitellus adocetus feeds on eight plant species and its burrows are grouped together. Our observations suggested that N. adocetus is not very social. Two reproductive periods were observed in those living among crops and one in tropical deciduous forest.

RESUMEN

Registro de una población y descripción de algunos aspectos de historia de vida de Notocitellus adocetus en el norte del estado de Guerrero, México.

Notocitellus adocetus es un roedor endémico de México, con poca información sobre su historia de vida. Describimos una población de N. adocetus que vive el norte de Guerrero y proporcionamos información de algunos aspectos de su biología. Se realizaron registros de la especie de junio del 2015 hasta octubre del 2017. Esta especie presentó actividad durante todo el día en los cultivos de maíz, pero no en el bosque tropical deciduo. Notocitellus adocetus consume ocho especies de plantas y sus madrigueras presentan un acomodo en agrupaciones. El número de individuos interactuando durante el estudio sugiere que N. adocetus no es social. Dos períodos reproductivos fueron observados en aquellos que viven en los cultivos y uno en el bosque tropical caducifolio.

Key words: Behavior; Corn crop; Feeding; Reproduction; Tropical deciduous forest.

Palabras clave: Alimentación; Bosque tropical caducifolio; Cultivo de maíz; Conducta; Reproducción.

Recibido 22 enero 2018.
Aceptado 25 abril 2018.

Editor asociado: S. Solari


Squirrels (Sciuridae) are currently represented by 35 species in Mexico, 13 of which are endemic (Ramírez-Pulido et al. 2014; Sánchez-Cordero et al. 2014). Most of these have wide distributions, though several endemic species (such as Spermophilus perotensis, S. madrensis, Cynomys mexicanus, Tamiasciurus mearnsi, C. ludovicianus and Notocitellus adocetus)are restricted to specific habitats (Valdés 2003). N. adocetus is a terrestrial squirrel restricted to the states of Mexico, Guerrero, Michoacán and Jalisco (Villa-Ramírez et al. 1991; Best 1995; Thorington et al. 2012; Valdéz & Ceballos 2014). This species inhabits dry and rocky environments, such as xerophilous scrub and tropical deciduous forest (TDF), is associated with farmlands, and may be found between 200 to 1200 m a.s.l. (Thorington et al. 2012; Valdéz & Ceballos 2014).

Notocitellus adocetus feeds on the fruits and seeds of Crescentia alata, Acacia cochlyacanta, A.  farnesiana, Prosopis jugiflora and Pithecellobium dulce, as well as those of corn, sorghum and beans. Notocitellus adocetus has been observed invading farmlands in seasons when food is scarce in TDF (Villa-Ramírez et al. 1991; Valdéz & Ceballos 2014). No study has been conducted on the associations between these plants and sciurids in the environments they inhabit.

Most species of Notocitellus are polygynous and have annual reproductive cycles, and N.  annulatus and N. adocetus can be estivate during the hottest months (Yensen & Sherman 2003). Notocitellus adocetus reproduces throughout the year in farmlands, whereas in TDF, it reproduces at the end of the dry season (from May to June) when the production of fruits and seeds is high (Valdéz & Ceballos 2014). Notocitellus have litter sizes of 4-9 depending on the altitude (Armitage 1981), food availability, abundance of predators, tree density and population density (Dobson & Murie 1987; Karels et al. 2000). Burrows can be occupied by one adult individual with its young, and the burrows can have more than one entrance and several chambers (Yensen & Sherman 2003).

Lacey et al. (1997) reported that the density of ground squirrels is from 13 to 16 individuals/ ha; Villa-Ramírez et al. (1991) indicated that N. adocetus populations are abundant in some regions of the states of Michoacán, Guerrero and Jalisco.

Here, we confirm the presence of N.  adocetus in the municipalities of Zirándaro de los Chávez in Guerrero and Tejupilco in Mexico. We studied the population in the north of Guerrero and provide information on some aspects of its life history, such as the number of individuals, feeding habits and reproduction.

The study was carried out at the Cuambio locality in the municipality of Zirándaro de los Chávez, Guerrero. The study site is located between 18° 25¢ 49.38² North Latitude and 100° 59¢ 38.70² West Latitude, in the Río Balsas basin, between 209 to 324 m a.s.l. Average annual temperature is 28.9° C and annual average rainfall is 977.2 mm (from 1951 to 2010), with eight lower precipitation months (October through May) (Conagua 2017). Vegetation is tropical deciduous forest (TDF) (Figueroa et al. 2009; INEGI 2009). Some areas are used for temporary and irrigation crops to farm maize, sorghum, sesame and, to a lesser degree, mango, plum watermelon, cantaloupe, squash, cucumber, tomato, chili, hibiscus and beans, in addition to cattle grazing (Duque, pers. comm.;O. Mendoza, in prep.).

Prior to this study, we recorded three individuals of N. adocetus (one in September 2015 and two in October 2017) in the municipality of Tejupilco, in the state of Mexico (18° 47¢ 16.90² North Latitude and 100° 23¢ 48.12² West Latitude). Also, before conducting our study, we observed three individuals in June 2015 and two in March 2016 in TDF at our study site in the Cuambio locality in Guerrero, as well as six individuals in June 2016 in areas with irrigation corn crops.

Sampling in TDF was performed during the dry season (January through May 2017), because more food resources are produced during this period at this site (Murphy & Lugo 1986); as for corn crops (irrigation areas), sampling was conducted in September and October 2016, since they produce throughout the year.

The presence of N. adocetus was recorded in corn crops in September and October 2016 and in TDF in January, March and May 2017. Direct records were obtained every hour by walking through each zone from 8:00 to 18:00  h along two transects; one in the 1.70 km corn crops areas and another in the 1.10 km long TDF (Bello & Hidalgo 2009; Corlatti et al. 2017). We recorded the time of activity, plant species on which it fed and some reproductive aspects. We also placed three digital trap cameras (Bushnell Trophy cam HD, Essential E2) at each site during the sampling.

We counted active and inactive burrows in corn crops and TDF in three 50 x 20 m plots in each area, following the method established by Bean et al. (2012), who estimated abundance of Kangaroo rats by counting active burrows. Three plots measuring 3 x 10 m were set to determine the architecture of the N. adocetus burrows in corn crops and TDF, where we marked the distance to the nearest burrow, the entrance diameter and orientation and the material used by squirrels to build their burrows (soil, rocks, tree trunks, etc.). We also measured the depth of the burrows in corn crop areas (Meliyo et al. 2014; Fenner et al. 2012).

Presence of juveniles was determined by indirect measurements using fine soil traps measuring 1 m2 covered by a single 3-cm layer of previously sifted dirt (Murillo & Giraldo 2011) in each study area. Twenty-four traps were placed in corn crops in September and October 2016. In TDF, twelve were set in January and March 2017 and six in May 2017.

We recorded a greater number of individuals in the transects laid in corn crops than those in TDF during the sampled months (Corn crop: 31; TDF: 13). Squirrels were most active from 9:00 to 14:00 h in TDF, with peak activity at 12:00 h, whereas in corn crops it is active almost all day, from 9:00 to 18:00 h, with highest activity at 13:00 h and then again at 17:00 h (X2 = 66.45, df = 10, P < 0.0001; Fig.  1). These periods of activity are similar to those reported for this species by Valdéz & Ceballos (2014), who found that the periods of greatest activity occur from 9:00 to 11:00 h. Greater activity at the corn crop sites may be due to greater food availability (Addisu & Bekele 2014; Kotler 2014). Furthermore, the corn crops are located in an old alluvial terrace with a fluvisol-type soil, with influence of the phreatic zone due to the proximity of the Río Chiquito, and the presence of native trees around the corn crops sites, could influence that this site be more fresh, humid and shaded (O. Mendoza, in prep.).


Fig. 1
Variation per hour in number of sightings of N. adocetus in corn crops and TDF, in Cuambio, Guerrero, Mexico.

We found 46 burrows in corn crops, of which 71.74% were active and 49 burrows in TDF, of which 75.51% were active, by sampling 3600  m2 in each habitat. These differences were not significant (F2,11 = 0.7924, P > 0.05; Fig. 2).


Fig. 2
. Mean number and standard error of active and inactive burrows observed in corn crops and TDF.

Notocitellus adocetus burrows are clumped into groups. Distance to the nearest burrow was 178.98 cm (± 20.1 cm) in corn crops, whereas it was 139.72 cm (± 20.8 cm) in TDF (U = 296, P > 0.05). Distance between burrows ranges from 90 to 289 cm in corn crops, and from 85 to 154 cm in TDF (Fig. 3).


Fig. 3
. Box plot showing mean distance (black point) to the nearest burrow in corn crops and TDF. Vertical lines (“whiskers²) represent the maximum and minimum values of the data set, the horizontal lines inside the boxes represent the medians of the data set, and the boxes represent the interquartile range.

We found that burrows in corn crops were 46.66 cm (± 4.07 cm) deep, which is similar to those of the mole rat Fukomys damarensis (Thomas et al. 2016) and the Indian gerbil Tatera indica (Adarsh 2013). It was not possible to measure the depth of burrows in TDF because they have several interconnected entrances and the shape of the burrows and tunnels is very irregular, similar to those observed for squirrels Otospermophilus beecheyi and Thomomys bottae (Miller 1957; VerCauteren et al. 2002; Adarsh 2013). The length and dimensions of the burrow entrances depend on the type of soil as observed in O. beecheyi (Van Vuren & Ordeñana 2012).

Continuing with the description of burrow architecture, we found that the entrance area of N. adocetus burrows in corn crops and TDF is similar (corn crops: 41.57 ± 4.70 cm2; TDF: 43.16± 3.55 cm2), much the same as F.  damarensis, Bandicota bengalensis, T.  indica, and Rattus sp. (Adarsh 2013; Thomas et al. 2016). We found that burrow entrances in corn crops mostly face east, whereas they face southwest in TDF, possibly because the incidence of sunrays is lower in this direction at morning, and noon in the latter (Murrieta-Galindo & Cuautle-García 2016).

The soil in corn crops is clayish and eroded, unlike TDF, where burrows are located in holes between rocks and under both live and dead trees. Ground squirrels can potentially use burrows built by other animals, as is the case of Xerus inauris using burrows of the aardvark Orycteropus afer in southern Africa (Whittington-Jones et al. 2011; Ewacha et al. 2016).

In corn crops, we observed that N.  adocetus feed on corn seeds (Zea mays), mango pulp (Mangifera indica), plum (Spondias purpurea), the stems, roots and tubers of grass “coquillo² (Cyperus rotundus), and the pulp and seeds of “cirián² (Crescentia alata). It is known that most rodents might include corn in their diets, thus becoming a potential pest and damaging crops (Houtcooper 1978; Moran & Keidar 1993; Bekele & Leirs 1997; Del Villar-González 2000; Sarwar 2015). In TDF, we observed that N.  adocetus feeds on the pulp and seeds of “cirian² (C. alata) and the pulp and seeds of “tecuche² (R. capitata), and we indirectly observed that it feeds on the seeds of “cascalote² (Caesalpinia coriaria) and “chucumpú² (Cyrtocarpa procera). Direct observations and digital trap cameras indicated that N. adocetus ingest seeds in situ and carry them in its cheek pouches to the nearest burrow for storage and subsequent consumption.

In TDF, we observed squirrels competing with individuals of the same species for food, as described for genera Notocitellus and Amnospermophilus(Yensen & Sherman 2003). Digital trap cameras registered antagonistic relationships between males of N. adocetus, in which dominant males aggressively drove away other individuals of the same sex, and also scared away and stole food from females, though on rare occasions these males allowed females to feed on the same fruit. We observed that females of N. adocetus also antagonize each other while feeding, though not as aggressively as males. This type of behavior is mainly due to competition for food or sexual selection (Lovejoy & Barsyte 2011).

In October 2017, we observed lone individuals of N. adocetus (seldomly in pairs), or couples with a young (1.42 ± 0.17 individuals per burrow). In TDF, we found small footprints (in two fine soil traps) three times in March 2017. In May 2017, we found a trail of small footprints (in two fine soil traps) and observed one young in transects. In corn crops, we found four sets of small footprints left by young (in four fine soil traps) in October 2016, and observed two juveniles and one female with clearly developed mammary glands in October 2017. This suggests that this species has at least two reproductive periods when living in crops, which does not match what was reported by Valdéz & Ceballos (2014) in farmlands. According to Moore et al. (1934), this characteristic is common in rodents such as Xerus inauris, whose females do not hibernate and are thus receptive throughout the year (Waterman 1998). Presence of irrigation crop zones can provide food resources throughout the year and favor the existence of more than one reproductive period in N. adocetus.

The present study adds to the knowledge of some aspects of the life history of N. adocetus, although more studies are needed to learn more of this endemic species, specifically density of individuals, population status, reproductive cycle and availability of food resources throughout the year in both environments. The role of N. adocetus in the zone should also be studied, since the locals believe that it harms crops, which could place these populations at risk.

Acknowledgments

Funding assistance for the project was provided by FESI-DIP-PAPCA-2016-4 to MF Ramos-Ordoñez and AM Contreras-González. We thank Irais Duque Díaz, Marleth S. Mendoza Orozco, Jesus Ortega Esquinca, Edgar Yafhed Martínez, Osman Rogelio Díaz González, David Adolfo Mota Aldrete and Hernández Yael Reyes Cruz for their help with the fieldwork. We also thank Sergio Díaz Infante Maldonado and María Felix Ramos-Ordoñez for lending digital trap cameras.

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