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A Population Study of the House Mouse, Mus musculus (Rodentia: Muridae), in a Rural Community of Mérida, México
Jesús Alonso Panti-May, Silvia F. Hernández-Betancourt, Marco A. Torres-Castro, Julián Parada-López, Sandra G. López-Manzanero, and Maribel C. Herrera-Meza

Caribbean Naturalist, No. 46

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Caribbean Naturalist 1 J.A. Panti-May, et al. 22001188 CARIBBEAN NATURALIST No. 46N:1o–. 1436 A Population Study of the House Mouse, Mus musculus (Rodentia: Muridae), in a Rural Community of Mérida, México Jesús Alonso Panti-May1,*, Silvia F. Hernández-Betancourt2, Marco A. Torres-Castro3, Julián Parada-López2, Sandra G. López-Manzanero2, and Maribel C. Herrera-Meza2 Abstract - The design of an integrative pest management program for rodents depends on an understanding of the biology and ecology of pest species. Here, we describe the abundance, and demographic and reproductive parameters of Mus musculus (House Mouse) in Mérida, Yucatán, México. A total of 906 house mice were trapped over 3 dry seasons (2009–2014) in a rural community. The sex ratio was significantly different from 1:1, with males (n = 519) more abundant than females (n = 389). Male mice were heavier than nonpregnant females. Mice in the weight class 8.1–12.0 g were more abundant compared to other weight classes. House Mice trapped in Mérida had high reproductive parameters (e.g., 51% of females were pregnant) and reproductive rates (estimated birth rate of 61 young per year). This information provides additional insights into the natural history of the House Mouse in tropical regions. Further studies evaluating factors such as rainfall, pathogens, or predation rates on mouse populations will increase our understanding of rodent population dynamics in tropical rural localities. Introduction Knowledge of the biology, ecology, and behavior of commensal rodents is an important component for the design and development of integrative management programs (Singleton et al. 2001). Moreover, this information is basic to understand rodent-borne disease transmission and for any integrated public health response to established or emerging zoonotic diseases (Mills and Childs 1998). Recent studies in Mérida, Yucatán, México, have reported that zoonotic pathogens such as Leptospira (Torres-Castro et al. 2014), flavivirus (Cigarroa-Toledo et al. 2016), and Hymenolepsis diminuta (Rudolphi) (Rat Tapeworm; Panti-May et al. 2017) circulate among commensal rodents. These studies have shown that pathogens harbored by rodents could be a potential health risk for inhabitants. Mus musculus L (Rodentia: Muridae) (House Mouse) is one of the most widespread mammals in the world, being found in both tropical and temperate regions 1Doctorado en Ciencias Agropecuarias, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Km 15.5 Carretera Mérida-Xmatkuil, C.P. 97135, Mérida, Yucatán, México. 2Departamento de Zoología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Km 15.5 carretera Mérida-Xmatkuil, C.P. 97135, Mérida, Yucatán, México. 3Laboratorio de Enfermedades Emergentes y Reemergentes, Centro de Investigaciones Regionales “Dr. Hideyo Noguchi”, Universidad Autónoma de Yucatán, Av Itzáes #490 x 59, Centro, C.P. 97000, Mérida, Yucatán, México. *Corresponding author - panti.alonso@gmail.com. Manuscript Editor: Angelo Soto-Centeno Caribbean Naturalist J.A. Panti-May, et al. 2018 No. 46 2 (Latham and Mason 2004). This species is also considered one of the most important pests in urban and rural environments. It can occur in a wide variety of habitats; however, in anthropogenic habitats such as cities, rural communities, and farms, it persists by continuously using shelter and food provided by humans (Pocock et al. 2004). The success of the House Mouse in these habitats has been attributed to its commensal behavior and its adaptability (Vadell et al. 2014). Human residences are ideal habitats where the House Mouse finds stable environmental conditions (e.g., temperature, humidity) and abundant food supplies, which favor its reproduction throughout the year (Pocock et al. 2004). However, human disturbance can rapidly change these conditions (Pocock et al. 2004), and thus modify the population dynamics of the House Mouse. In a previous study, Panti-May et al. (2012) reported that the House Mouse was the most abundant species in a rural community of Yucatán and that it had high reproductive proportions. Additionally, reports from epidemiological studies on rodent-borne diseases have reported that this rodent is prevalent in several rural areas of Yucatán and harbor several zoonotic agents (Panti-May et al. 2015, 2017; Torres-Castro et al. 2014, 2016). Despite the medical and economic importance of rodents in tropical regions of America, most ecological studies of House Mice have been focused on urban populations restricted to temperate regions (Brown 1953, Gomez et al. 2008, King 1950, Vadell et al. 2010). The lack of studies describing the population characteristics of the House Mouse from tropical latitudes has limited our knowledge regarding the demography, reproduction, and growth patterns, especially in commensal habitats. In addition, Bergmann’s rule, which states that endothermic species from cooler environments tend to be larger than congeners from warmer environments, marks the importance of avoiding generalizations of commensal rodents sampled from different latitudes (Berry and Scriven 2005, Porter et al. 2015). The aim of this paper was to study the population characteristics of the House Mouse in a commensal habitat in a tropical area and its variations between years and with temperate environments. We conducted rodent trapping in households of a rural community in Mérida to test 2 hypotheses. First, reproduction and growth of the House Mouse in a commensal and stable habitat occur without variations throughout the years. We expected no marked differences in abundance and demographic and reproductive parameters of House Mice in 3 dry seasons. Second, reproduction and growth of House Mice from tropical regions differ from those of their temperate congeners. We expected lower reproductive rates and weights in tropical House Mice than those reported from temperate regions. Materials and Methods Study site This study was carried out in the community of Molas (20°48'55"N, 89°37'55"W), located in a rural area in the municipality of Mérida, Yucatán, México. Molas is ~30,000 m2 in area, has 2014 inhabitants, and is located within the Cuxtal Ecological Reserve, where the vegetation is representative of a low deciduous tropical Caribbean Naturalist 3 J.A. Panti-May, et al. 2018 No. 46 forest (Instituto Nacional de Estadística y Geografía 2012). The regional climate is warm, sub-humid with average temperatures of 29 °C in July and 24 °C in January; the annual precipitation is 1100 mm, with the dry season from October to May averaging 300 mm, and a wet season occurring from June to September averaging 900 mm (White and Hood 2004). The majority of houses are small with solid floors, walls, and ceilings, but these are generally in poor condition with cracks and holes. Some families have rooms or houses constructed with stones and wooden poles and thatched with cardboard sheets. In general, yards surrounding the houses are large and bounded by stone walls, known locally as “albarradas”. It is common to find pets (i.e., dogs and cats), domestic animals (i.e., chickens, turkeys, pigs, sheep, cattle, and horses), unserviceable domestic appliances, and volumes of vegetation (i.e., weeds, shrubs, trees, and vegetable patch plots) in the yards (see Fig. 1). We divided the community into 2 homogeneous sectors to facilitate the trapping. Initially, in each sector, we randomly selected 20 households by using satellite maps of the community. However, at the end of seasons 1 and 2, some of the families could not continue with the study and so for each of them we invited a neighbot to participate in their place but still used the data acquired from those who had moved. Thus, the final number of households involved in the study was 52 (Fig. 2). Trapping methodology We trapped rodents over 3 dry seasons (DS) as follow: DS1 = October 2009 to April 2010, DS2 = October 2011 to March 2012, and DS3 = November 2013 to April 2014. We did not conduct rodent trapping in rainy seasons because our previous experiences demonstrated that rains relut in a high percentage of sprung traps. In each household, 12 (DS1 and DS2) or 8 (DS3) Sherman traps (2 sizes were used: 8 cm x 9 cm x 23 cm and 8 cm x 9.5 cm x 30.5 cm; HB Sherman Traps, Inc., Tallahassee, FL, USA) were set for 3 consecutive nights. We baited the traps with a mixture of oatmeal and vanilla essence and placed them inside houses and yards close to signs of rodent activity (fecal dropping, burrows, or active runs) and potential sources of food (exposed garbage and human or animal food) or harborage (areas with vegetative coverage and unserviceable domestic appliances). We transported trapped rodents to the laboratory for euthanization with an intraperitoneal injection of sodium pentobarbital (130 mg/kg; Pisabental®, PISA Agropecuaria). Field and laboratory rodent procedures were carried out following the guidelines of the American Society of Mammalogists for the use of wild mammals in research (Sikes et al. 2011), the guidelines of the American Veterinary Medical Association for the euthanasia of animals (Leary et al. 2013), and also national specifications (Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación 1999). The rodent trapping was conducted under license from the Mexican Ministry of Environment (SGPA/DGVS/02528/13). Data collection After euthanasia, we recorded the specimens’ species identification, sex, and weight. We classified females as mature when (1) the vagina was open, (2) the specimen was pregnant (by visible embryos) or (3) lactation was evident (by presence Caribbean Naturalist J.A. Panti-May, et al. 2018 No. 46 4 of milk). We considered males that had scrotal testicles to be mature. We recoreded pregnant and/or lactating females as parous. Trap success was used to estimate the relative rodent abundance as follows: (number of House Mice trapped) x 100 / (number of traps x number of nights) (Gómez Villafañe et al. 2013). Data analysis We used a chi-squared test with Yates’s correction to determine whether the sex ratio varied from parity (Zar 1996), and the parametric Welch 2-sample t-test Figure 1. Characteristics of households sampled in the community of Molas, Mérida, México. Photographs of typical households illustrating the conditions of (A–C) houses, walls, windows, fences, and the front yard, as well as (D–F) the amount of vegetation, henhouses, pigpens, unserviceable domestic appliances present in backyards. Caribbean Naturalist 5 J.A. Panti-May, et al. 2018 No. 46 to asess whether the mean weight was significantly different between seasons and between sexes. Additionally, the weight of each specimen was classified in one of seven 4-g classes to determine whether the cumulative proportion differed between sexes using the 2-sample Kolmogorov-Smirnov test (Sheskin 2004). We compared the proportion of sexually active House Mice between seasons and sexes. All statistical analyses were performed in R (R Core Team 2014), using the package stats and a P < 0.05 level of significance. To estimate the number of births per female House Mouse over the total trapping days, we used the formula (Emlen and Davis 1948): F = I x t / 14.5, where F = frequency of pregnancy, I = incidence of visible embryos, t = sampling days, and 14.5 = the number of days embryos are visible out of the estimated 19.5 days of gestation (Laurie1946). Using the solution for F, we estimated the total number of House Mice entering the population by multiplying by the average number of embryos per pregnant female (corrected with the average loss of embryos). Considering that reproductive parameters of rodents living in commensal habitats, such Figure 2. Spatial distribution of households where House Mouse trapping was performed. Dark dots represent households where House Mice were trapped over the course of the 3 dry seasons and grey dots represent households where trapping was performed during 1 or 2 seasons. Caribbean Naturalist J.A. Panti-May, et al. 2018 No. 46 6 as residential areas, with stable micro-environmental conditions and abundant food supplies do not show marked seasonal changes (Panti-May et al. 2016a, Pocock et al. 2004), the annual productivity in terms of the number of young can be estimated by extrapolation (Emlen and Davis 1948). Results A total of 1210 rodents (411 in DS1, 461 in DS2, and 338 in DS3) were captured during the 22,788 trap-nights. The House Mouse was the most abundant species (906 specimens, 74.9%), followed by Rattus rattus L. (Rodentia: Muridae) (Black Rat; 175 specimens, 14.5%) and 6 native species of 2 families, Cricetidae (126 specimens, 10.4%: 96 Peromyscus yucatanicus Allen and Chapman [Yucatán Deer Mouse], 12 Ototylomys phyllotis Merriam [Big-eared Climbing Rat], 10 Sigmodon toltecus (de Saussure) [Toltec Cotton Rat], 7 Reithrodontomys gracilis Allen and Chapman [Slender Harvest Mouse], and 1 Peromyscus leucopus (Rafinesque) [White-footed Mouse]) and Heteromyidae (3 Heteromys gaumeri Allen and Chapman [Gaumer’s Spiny Pocket], 0.2%). All native species were trapped in the yards of households located in the periphery and associated with patches of secondary forest surrounding the community. The House Mouse was frequently trapped in yards (65.7%) close to henhouses, fences, and areas with vegetation cover (e.g., vegetable patch plots), while the remaining (34.3%) individuals were trapped inside houses in bedrooms, kitchens, and places where food was stored. The overall trap success of the House Mouse was 4.1%. Since population characteristics of House Mice were similar between DS1, DS2, and DS3, we pooled data into 1 group (Table 1). The ratio of female (n = 386) to male (n = 519) House Mice significantly differed from parity (χ2 1 = 19.5, P < 0.001). However, this difference was found only in DS1 (χ2 1 = 18.9, P < 0.001), whereas the ratio in DS2 (χ2 1 = 3.5, P = 0.06) and DS3 (χ2 1 = 1.7, P = 0.19) was not significantly different from 1:1. The mean weight of pregnant females, 13.9 ± 0.3 g (± standard error) was significantly greater than the 10.9 ± 0.2 g of non-pregnant females (t383 = 8.7, P < 0.001). Additionally, males were heavier than non-pregnant females (11.4 vs 10.9 g; t772 = 2.7, P = 0.007). However, there were no statistical differences in the weight structure between non-pregnant females and males (D = 0.08, P = 0.18). Of all the weight classes, 8.1–12.0 g had the most mice (Fig. 3). The percentage of mature males (86.9%) was higher than that of mature females (38.3%) (χ2 1 = 230.5, P < 0.001). The percentages of pregnant and lactating females were 59.5% and 13.5%, respectively. The mean number of embryos per pregnant female was 4.5 ± 0.1. All parous females weighed ≥9 g. Table 1 shows the summary of population characteristics of House Mice in Mérida. As the proportion of mature, pregnant, and lactating females were similar between the 3 dry seasons, we estimated the pregnancy frequency for the House Mouse. The parameters were I = 0.571 and t = 176 sampling days. Using these values, the frequency of births for the House Mouse was 6.9. Correcting these values for 3% intrauterine loss of entire litters (Emlen and Davis 1948), a Caribbean Naturalist 7 J.A. Panti-May, et al. 2018 No. 46 Table 1. Summary of population characteristics of the House Mouse for each dry season (DS) in Mérida, México. SE = standard error. Characteristic n DS 2009–2010 n DS 2011–2012 n DS 2013–2014 n Total No. of mice (%) Females 122 (37.9) 169 (45.2) 95 (45.5) 386 (42.7) Males 200 (62.1) 205 (54.8) 114 (54.5) 519 (57.3)D Mean (SE) weight (grams) Non-pregnant females 86 10.8 (0.3) 136 11.1 (0.3) 72 10.6 (0.3) 294 10.9 (0.2)D Males 200 11.4 (0.2) 205 11.4 (0.2) 114 11.6 (0.3) 519 11.4 (0.2) Pregnant females 32 13.5 (0.5) 33 14.1 (0.5) 23 14.4 (0.7) 88 13.9 (0.3) No. of mature (%) males A 196 177 (90.3) 204 168 (82.4) 114 102 (89.5) 514 447 (86.9) No. of mature (%) females 122 58 (47.5) 169 48 (28.4)C 95 42 (44.2) 386 154 (39.9) No. of lactating (%) femalesB 58 9 (15.5) 48 6 (12.5) 42 5 (11.9) 154 20 (13.8) No. of females visibly pregnant (%)B 58 32 (55.2) 48 33 (68.7) 42 23 (54.8) 154 88 (57.1) Mean number (SE) of embryos 30 4.6 (0.2) 33 4.3 (0.3) 21 4.5 (0.3) 84 4.5 (0.1) Median trap success (range) 6 3.6 (3.2–4.9) 6 4.7 (2.9–5.0) 6 3.6 (2.9–5.3) 18 4.1 (2.9–5.3) AValues shown for number of males (n) in this row does not always match the value provided above for total number of male mice because for some of the specimens, the maturity section was mistakenly left blank, and so those individuals were not included. BConsidering only mature females. CSignificant differences between DS1 and DS2 and between DS2 and DS3 at P < 0.05. DSignificant differences from Total column between non-pregnant females and males at P < 0.05. Caribbean Naturalist J.A. Panti-May, et al. 2018 No. 46 8 mature female brought, on average, 6.7 viable litters to birth over the sampling period. The estimated interval between births was 26 days. The mean number of embryos (4.5) per pregnant female was corrected for 3% embryos mortality (Laurie 1946). The estimated annual productivity for a mature female was 61 young (1 young every 6 days). Discussion The reproductive rate and size of a rodent population is dependent on factors such as food and shelter (Channon et al. 2006). In commensal habitats composed mostly of human-arranged materials (e.g., residential areas), food and shelter sources are more abundant and accessible for rodents compared with non-commensal habitats (e.g., natural areas) (Castillo et al. 2003, Pocock et al. 2004). In these habitats, House Mice do not move more than 3–10 m and usually establish their colonies inside or close to dwellings (Battersby et al. 2008). These factors can explain the lack of variability in abundances and demographic and reproductive parameters found in House Mice over 3 years in Mérida. In addition, the low-level sanitation practices and the lack of garbage collection service can also contribute to abundant House Mouse populations. In this study, the sex ratio was significantly different than 1:1 in DS1 (males were more abundant than females), but not in DS2 and DS3. The adjustment in the sex ratio of young is a facultative capacity of polygynous animals (Trivers and Figure 3. Comparison of weight classes between non-pregnant female and male House Mice from Mérida, México. Black bars = females and grey bars = males. Caribbean Naturalist 9 J.A. Panti-May, et al. 2018 No. 46 Willard 1973). Studies on laboratory mice have shown that maternal nutrition can affect the sex ratio and viability of young (Rosenfeld and Roberts 2004). In rodents, parity has been reported when food is nutritionally balanced and ad libitum, whereas under deficient and/or restricted diets, females produce a male-biased sex ratio (Rosenfeld and Roberts 2004, Wright et al. 1988). This finding suggests that rural households offer a moderately stable habitat for commensal rodents with abundant and accessible food, favoring a sex ratio of 1:1. The reasons for the male-biased sex ratio found in DS1 are not clear, but could be associated with factors such as juvenile mortality, male dispersal, inbreeding, or population density (Clutton-Brock and Iason 1986). Body size is the result of both natural and sexual selection (Schulte-Hostedde 2007). All of the selection pressures acting on males and females dictate the direction and magnitude of sexual size dimorphism (Schulte-Hostedde 2007). In this study, we found that male mice were significantly heavier (11.4 g) than females (10.9 g). Sexual size dimorphism is expected to be male-biased in polygynous rodents, such as Mus, that have constant male–male competition for dominance hierarchies and estrous females (Berdoy and Drickamer 2007). In addition, we also found that mature males were more abundant than mature females, which is consistent with results from urban populations in the city of Mérida, México (Panti-May et al. 2016b). The results obtained in this study showed that House Mice in Mérida had high reproductive rates. The House Mouse had an estimated pregnancy frequency of 6.7, an interval between litters of 26 days, and an annual productivity of 61 young. The poor conditions prevalent in the households sampled could favor an abundance of food and shelter sources that would allow for House Mouse reproduction throughout the year. However, further studies examining factors such as seasonality, mortality, and migration, could improve our understanding of the ecology of the House Mouse from tropical regions. The life history of an organism typically consists of patterns of growth, reproduction, and survival (Dobson and Oli 2007). These characteristics are vital to the ecology of the organism because life history reveals how populations are adapted to their environment or how they respond to changes in environment (Dobson and Oli 2007, Vadell et al. 2014). The number of embryos per pregnant female (4.5) found in this study was smaller than those reported for House Mice in temperate regions. In Mississippi, USA, Smith (1954) reported 4.9 and 5.0 embryos in female House Mice trapped in residences and food-handling establishments, respectively. In cultivated regions of central Argentina, Mills et al. (1992) found that female House Mice had 6.2 embryos. In London, UK, Laurie (1946) reported 5.2, 5.5, and 5.9 embryos per pregnant female House Mouse from urban habitats, buffer depots, and corn-ricks, respectively. Another important difference in tropical vs. temperate House Mouse populations was the lower proportion of heavy individuals (>16 g) from Mérida (2.5%) compared with the 26.0% reported in Baltimore, USA (Brown 1953), and the 22.0–28.2% found in London (Laurie 1946). These differences suggest that tropical and temperate mice can differ with respect to body metrics and Caribbean Naturalist J.A. Panti-May, et al. 2018 No. 46 10 reproductive parameters, as has been reported in Rattus norvegicus (Norway Rat; Porter et al. 2015). In this study, we recorded 6 native species in backyards of households located on the periphery of the study site. Notably, the Yucatán Deer Mouse was recorded with a relatively high number of specimens (96) in the 3 seasons. This species is widely distributed in Yucatán, and it is common in tropical forests, secondary patch forests, and grain fields. Its omnivorous feeding and reproductive strategies (i.e., high litter size, short gestation period, and early age at maturity) provides advantages for colonizing unstable habitats (Young and Jones 1983). Thus, it is possible that this native species may exert competitive pressure on the House Mouse (Gomez et al. 2008). Even though our study was limited to dry seasons and sampling was restricted to a single rural community, these findings are critical and contribute to the knowledge of rodent ecology in tropical environments of America. The existing data from temperate populations inhabiting commensal habitats (e.g., households, industries, or farms) show that the House Mouse is non-seasonal breeder but often has reproductive peaks in the fall and spring (Brown 1953, Smith 1954). In tropical zones, seasonal reproduction of small mammals in sylvan environments is related to rainfall and food availability (Bergallo and Magnusson 1999). A study in Salvador, Brazil, reported that abundance and reproductive parameters of Norway Rats were similar between dry and rainy seasons (Panti-May et al. 2016a). However, the lack of data from rainy seasons limited our understanding regarding their seasonal reproduction. In conclusion, our results indicate that the House Mouse from Mérida, México, had high reproductive rates during the dry seasons. We also found reproductive and body size differences compared with data reported for temperate populations. Although this study has limitations, the information generated is relevant for the understanding of the ecology of mice in tropical regions. This information should be considered in studies of rodent-associated zoonoses and integrative programs for rodent control. Further studies evaluating factors such as rainfall, pathogens, or predation rates on House Mice and utilizing data from a whole life-cycle and gathered over several years will increase our understanding of population dynamics in tropical rural localities. Acknowledgments We thank all the families who participated in this research for their cooperation over the sampling. We also thank all the students who participated in the field work. We are grateful to Josh Taylor for his critical reading of the manuscript and for the revision to English. This research was funded by PROMEP-MEXICO-103.5/09/1258 “Estudio Multidisciplinario para la identificación de variables asociadas a la transmisión de enfermedades transmitidas por vector y enfermedades zoonóticas en Yucatán”. J.A. Panti-May was supported by a doctoral grant from Consejo Nacional de Ciencia y Tecnología (259164). Literature Cited Battersby, S., R.B. Hischhorn, and B.R. Amman. 2008. Commensal rodents. Pp. 387–419, In X. Bonnefoy, H. Kampen, and K. Sweeney (Eds.). Public Health Significance of Urban Pests. World Health Organization, Copenhagen, Denmark. Caribbean Naturalist 11 J.A. Panti-May, et al. 2018 No. 46 Berdoy, M., and L.C. Drickamer. 2007. Comparative social organization and life history of Rattus and Mus. Pp. 380–392, In P.W. Sherman and J.O. Wolff (Eds.). Rodent Societies: An Ecological and Evolutionary Perspective. The University of Chicago Press, Chicago, IL, USA. Bergallo, H.G., and W.E. Magnusson. 1999. 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