Artículos

 

Extreme population fluctuation in the Northern Pygmy Mouse (Baiomys taylori) in southeastern Texas

 

Alisa A. Abuzeineh¹, Nancy E. McIntyre², Tyla S. Holsomback², Carl W. Dick³, and Robert D. Owen^2,4*

 

¹ Aquatic Station, Department of Biology, Texas State University, San Marcos, TX 78666 USA.

² Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409-3131 USA.

³ Department of Biology, Western Kentucky University, 1906 College Heights Blvd., Bowling Green, KY 42101 USA.

⁴ Martín Barrios 2230 c/ Pizarro, Barrio Republicano, Asunción, Paraguay. *Corresponding author contact rowen@tigo.com.py

 

Sometido: 5 de febrero de 2011
Revisado: 25 de marzo de 2011
Aceptado: 13 de abril de 2011

 

Abstract

The Northern Pygmy Mouse (Baiomys taylori) occurs throughout much of Mexico and into the southwestern United States, with its range currently expanding northward in the U.S. Despite documentation of species range expansion, there have been very few studies that have monitored population growth patterns in this species. During a 16-month mark-recapture study in coastal southeastern Texas, a striking fluctuation in densities of Pygmy Mouse populations was observed. The extreme population increase and decline was evaluated with respect to several biotic and abiotic variables postulated to affect rodent population levels. Highest population levels were preceded by high fruit and seed availability, and variation in 6-month cumulative precipitation totals explained 73.8% - 77.1% of the population variation in the study.

Key words: Baiomys taylori; cumulative precipitation; Northern Pygmy Mouse; population fluctuation; rapid population increase; Texas.

 

Resumen

El Ratón Pigmeo Norteño (Baiomys taylori) se encuentra en gran parte de México y en el suroeste de los Estados Unidos, con su distribución expandiendose hacia el norte en los EE.UU. A pesar de la documentación de su expansión distribucional, ha habido muy pocos estudios que han monitoreado los patrones de crecimiento poblacional en esta especie. Durante un estudio marca-recaptura de 16 meses en la costa sureste de Texas, se observó una fluctuación aguda en las densidades de las poblaciones del ratón pigmeo. El aumento extremo y el descenso posterior de la población fueron evaluados con respecto a algunos cuantas factores bióticos y abióticos postulados a afectar los niveles poblacionales. Los niveles mas altos fueron anticipadas por la disponibilidad alta de frutas y semillas, y la variación de precipitación cumulativa total explicó 73.8% - 77.1% de la variación poblacional en el estudio.

Palabras claves: Baiomys taylori; fluctuación poblacional; precipitación cumulativa; Ratón Pigmeo Norteño; subida poblacional rápida; Texas.

 

Introduction

The Northern Pygmy Mouse, Baiomys taylori (Thomas 1887), is the smallest rodent in North America (adult weight 6 - 9.5 g; Packard 1960, Hudson 1965). This granivorous / herbivorous species occurs in a wide variety of habitats with dense ground cover (Eshelman and Cameron 1987). Its distribution extends from central Mexico northward into the southwestern United States (Packard 1960, Packard 1969, Pitts and Smolen 1989, Choate et al. 1990, Stuart and Scott 1992, Tumlison et al. 1993, Brant and Dowler 2002).

Because the species' distribution has been expanding northward in recent decades (Choate et al. 1990, Brant and Dowler 2002, Green and Wilkins 2010), and such range expansion may hinge upon a population's ability to grow rapidly (Sakai et al. 2001), the northern pygmy mouse might be expected to be capable of rapid population growth. Females can conceive as early as 28 days of age and have a gestation period of 20-23 days (Hudson 1974), a mean time between litters of 27.6 days (Blair 1941), and a mean litter size of about 2.5 (range 1-5; Quadagno et al. 1970). In a 6-year study in eastern Texas, population densities for B. taylori were found to range from 6-84 mice / ha (Grant et al. 1985), and other studies have reported density values within this range (Raun and Wilks 1964; Petersen 1975; Gust and Schmidly 1986).

We used a mark-recapture design to monitor population abundance of B. taylori as part of a larger study of rodent communities and zoonoses in southeastern Texas (McIntyre et al. 2005; Abuzeineh et al. 2007; Holsomback et al. 2009; McIntyre et al. 2009). We discuss biotic and abiotic factors that may have facilitated the dramatic increase and subsequent precipitous decline in population abundance observed during our study.

 

Methods

This study was conducted at Peach Point Wildlife Management Area (now named Justin Hurst Wildlife Management Area--headquarters at 28^o56'58"N, 95^o26'18"W) in Brazoria County, Texas, from May 2002 to August 2003. We conducted 6 trapping sessions at approximately 3-month intervals (see Abuzeineh et al. 2007 for additional details of sampling). The climate is moderate, with average daily high temperatures of 13°C to 33°C (December and August, respectively), and December and August average lows of 8°C to 24°C , respectively. The area receives an average of 109.2 cm of precipitation per year, much of it (26.7 cm, or 24.4%) in August and September (Table 1).

Two study grids (Fig. 1) were established, each of which was ~1 ha in size. The grids were located ~1 km apart in old-field habitats. Grid One was irregularly shaped, bordered by a marsh, and contained 112 trap stations. Grid Two was rectangular with a narrow pond in the center, and had 101-109 trap stations depending on the water level of the pond during different trapping sessions.

Habitat structure was measured within a 3-m-radius circle centered on each trap location (Mclntyre et al. 2009), and each grid was characterized as a composite of these measurements. Plants were identified and percent coverage of 10 mutually exclusive categories (grass, forb, litter [duff], tree, shrub, bare ground, vine, coarse woody debris, water, reed) was measured, following the protocol of Bullock (1996). The availability of potential rodent food sources (fruits and seeds) was assessed during each trapping session by noting which plant species had fruits or seeds present. The availability of seeds was categorized each month as Very Low (<5% of plants with seeds), Low (5-25%), Medium (25-50%), or High (>50%). Fruits were noted as present or not.

On each grid, Sherman live-traps (7.5 x 9.0 x 23.0 cm) were spaced 10 m apart and baited with rolled oats and peanut butter. Traps were checked each morning and animals processed and released at the point of capture. Traps were opened and rebaited in late afternoon. The populations were sampled for 6 nights each trap session, except August and December 2002 (4 and 5 nights, respectively). Captured rodents were marked with a unique identification number using toe-clipping during the first sampling session period Following IACUC recommendations, passive integrated transponder (PIT) tagging was used in all subsequent sessions. Additionally, age (adult, subadult, or juvenile; determined by examining pelage and weight), sex, and trap station were recorded. Field protocols followed accepted guidelines (Animal Care and Use Committee, 1998) and were approved by the Texas Tech University Animal Care and Use Committee.

The software program MARK (White and Burnham 1999;) was used to estimate population abundances. The program assumes a closed population during a given trapping session. We used the Pollock and Otto (1983) model (M_bh), which estimates population sizes based on new and recaptured individuals, allowing both for different probabilities of capture between first capture and recaptures and inter-individual heterogeneity of capture (or recapture) probability. This and similar algorithms, based on temporal patterns of capture and recapture of individual rodents within closed populations, produce accurate estimates of population size, particularly with high numbers of captures and recaptures (Otis et al. 1978; White and Burnham 1999; Owen et al. 2010). However, when trapping success is relatively low (i.e., ≤ 10 individuals encountered), these and similar algorithms generally cannot produce reliable estimates; in these cases, the Minimum Number Known Alive (MNKA; i.e., the number of individuals actually encountered) method was used to estimate population size.

Monthly precipitation data were obtained from the KNMI climate explorer, from Galveston,TX (29.30^oN,94.80^oW,ca. 73 kmNEofourstudysite, inasimilarcoastal location), http://climexp.knmi.nl/getprcpall.cgi?someone@somewhere+72242+GALVESTON+. For each of our six sampling periods, cumulative precipitation was calculated for the preceding two through eight months (Table 1). R² values were calculated between each of these series of cumulative precipitation values and the estimated Baiomys population abundances, for both grids. R² values and associated P values were calculated using SAS ver. 9.2 (SAS Institute, Inc., Cary, NC).

 

Results

Both of the mark-recapture grids were dominated by grass and forb cover with few trees, but the two grids differed in terms of vegetative composition (Table 2). Grid One supported 31 - 34 species of plants, depending upon the season, and overall was dominated by bluestem (Andropogon sp.) and baccharis (Baccharis halimifolia). Grid Two supported 31 - 37 plant species and was composed primarily of balloonvine (Cardiospermum halicacabum), elderberry (Sambucus canadensis), and flatsedge (Cyperus sp.). More detailed vegetative descriptions may be found in McIntyre et al. (2005, 2009).

During August-October 2002, the area received considerably higher than average rainfall, after which precipitation levels returned to normal or lower than normal (Table 1). During these 3 months, total rainfall was 96.2 cm, or 269% of the average 3-month total of 35.7 cm.

May 2002 and 2003 demonstrated very low seed abundance, whereas August 2002 and 2003 showed very high seed abundance (especially among the grasses) as well as the presence of fruits (e.g., elderberry and various other shrubs, forbs, trees, and vines). December 2002 and March 2003 showed medium and low seed abundances, respectively (Fig. 2). These patterns corresponded to seasonal changes in plant phenology.

During our study, 110 Baiomys taylori were captured, with more individuals encountered on Grid Two than on Grid One. Grid One yielded no B. taylori during 4 of 6 trapping sessions (May 2002 and March, May, and August 2003), 5 individuals (3 adult females, 2 adult males) in August 2002, and 30 (12 adult females, 6 adult males, 12 subadults) in December 2002. Grid Two yielded no B. taylori during 3 of 6 trapping sessions (May 2002 and May and August 2003), 9 individuals (6 adult females, 3 adult males) in August 2002, 61 (24 adult females, 26 adult males, 11 subadults) in December 2002, and 5 (2 adult males, 3 subadults) in March 2003 (Fig. 2). In December 2002, population abundances were estimated at 54 ± 15.9 (±SE) on Grid One and 233 ± 119.2 (±SE) on Grid Two. For all other sampling sessions, the MNKA (number of animals encountered) was used as the best estimate of the population size.

R² values provided a measure of the proportion of the variance in population values which is explained by the cumulative precipitation levels for 2- to 8-month periods (Table 1). R² values were significant (a = 0.05) for both grids for the 5-, 6-, and 7-month cumulative precipitation values, and highest for 6-month levels (R² = 0.7710 for grid 1 and R² = 0.7384 for grid 2; Table 1).

 

Discussion

On both grids, Baiomys were not encountered in May 2002, were recorded in small numbers in August, then experienced a dramatic population increase by December, followed by a precipitous decline in 2003. These trends were noted on both of our mark-recapture grids. Animals marked on one grid were not captured at the other, nor were grid-marked animals caught on any of several ancillary trap lines that were placed in similar habitats (at least 100 m from the mark-recapture grids). Although the results from ancillary trap lines cannot be used to estimate population abundance, capture rates on these lines closely paralleled those on the mark-recapture grids. We therefore are confident that our population estimates were representative and that the trends we saw were general for the area, and not idiosyncratic to a particular grid or habitat type.

Relatively constant forb and grass compositions in the study area appear to provide a favorable environment year-round for breeding individuals. Additionally, we noted that high population abundance occurred in sampling sessions following high seed abundances and presence of fruits. Our vegetation data indicate that these fluctuations correspond well with seasonal changes in food availability. Small mammals consuming low-caloric foods (e.g., grasses and seeds) have greater energy constraints per unit mass relative to resting metabolic rates than do small mammals that utilize high-energy resources. Because there are varying benefits and costs associated with different food resources, a relationship between rodent diet and reproductive behaviors has been hypothesized (Kalcounis-Rüppell and Ribble 2007).

However, the vegetation data do not explain well why abundances were considerably lower (5 and 0 individuals in March 2003 on Grids One and Two, respectively) in seasons subsequent to the population increase. The decline is especially puzzling given that most subadult animals were encountered in December 2002, with a few also in March 2003, indicating that breeding was continuing during this period. Moreover, no subadult animals were encountered in August 2002, suggesting that the extreme population increase actually began after that trapping session, and therefore occurred in less than 4 months.

Although we cannot demonstrate a direct causal link between precipitation and population trends, we note a strong and consistent pattern in which a significant proportion of the variation in population levels is explained by the cumulative precipitation preceding each of our sampling sessions. The R² levels increased steadily to peak at 6-month cumulative values, then declined to 8-month (and presumably greater) levels.

The capacity of Baiomys taylori for early and rapid reproduction (Blair 1941, Quadagno et al. 1970, Hudson 1974) certainly contributed to the rapid increase in abundance for the species. As with any species, the historical range of B. taylori undoubtedly results both from the interaction of biotic and abiotic components of its environment, and species-specific life history traits, such as age at first reproduction and litter size. Further, population "pulses" such as that documented in this study, not only may be contributing to the current range expansion of B. taylori, but also may have higher-order effects within the trophic system of which it plays an integral role. Therefore, these dynamics are worthy of future evaluation in this and other small mammal populations, particularly across areas where climate patterns are highly variable, or are documented to be changing.

 

Acknowledgements

We thank J. Oetgen and M. Ealy at the Peach Point Wildlife Management Area for facilitating our work there. We also thank R. A. Nisbett, M. A. Houck, Y.-K. Chu, A. Nix, J. Vacca, N. de la Sancha, and H. G. Wang for assistance in the field. P. Smith, W. Lidicker, and two anonymous reviewers reviewed the manuscript, and provided helpful comments. Finally, we thank the Advanced Research Program for funding (grant 0036440140-2001 awarded to NEM and M. A. Houck).

 

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Nota

Editor asociado: William Z. Lidicker, Jr.