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Christopher Ross
Christopher Ross

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ABSTRACT: The aim of this study was to analyze the effects of parents on maturation and reproductive activity of spring-born females in fenced populations of Calomys musculinus, at the beginning of the breeding period. The field study was carried out in four 0.25-ha enclosures (two control and two experimental), each situated on natural pasture. This study had two periods: 1) Absence of fathers (AF) (from September 2003 to January 2004), and 2) Absence of mothers (AM) (from October 2004 to February 2005). In both periods, in control enclosures both parents remained with the offspring. During AF period, in experimental enclosures only the mothers remained with their offspring. In AM period, only the adult males remained with their offspring in experimental enclosures. Three trapping sessions of 8 successive nights every fortnight were carried out. Sexual maturation and reproductive activity of spring-born females were compared between treatments using repeated-measures ANOVA. The repeated measures factor was the age of young females. In both periods the number of spring-born females in each reproductive condition was independent of treatments. The females matured according to their physiological times (30-40 days of age). The removal of fathers and mothers did not affect either the timing of sexual maturation or the reproduction of C. musculinus spring-born females. Future research to test the effect of adult female density on juveniles should be done to test the same parameters.


Calomys musculinus is the dominant rodent species of central and north-western Argentina, and the reservoir of Junin virus, the etiological agent of Argentine hemorrhagic fever (AHF) (Mills and Childs, 1998). It inhabits Pampean agrarian ecosystems and is found in a variety of habitats including natural pastures, crop-field edges, cultivated fields undisturbed after harvest, border areas protected by wire enclosures with little agricultural disturbance, roadsides, and railway banks (Busch et al., 2000). C. musculinus populations are characterized by seasonal density changes, with low density during winter (16 mice/ha) and peaks during summer or early autumn (260 mice/ha) (Mills et al., 1991, 1992). The reproductive period of this species begins in mid-September and finishes at the end of April (Mills et al., 1998). C. musculinus has a short gestation length (21 days) and each female can produce many pups in her lifetime (6 pups per litter). Females show a high frequency of postpartum estrus, which implies that a new pregnancy may overlap with the lactation of the previously produced litter (Mills et al., 1992; Buzzio and Castro-Vasquez, 2002). Juveniles of C. musculinus reach sexual maturity between 30 and 40 days of age, with a mean weight close to 16.5g. (de Villafañe, 1981). In the laboratory, C. musculinus females typically build covered nests, males do not contribute to the construction of the nest, and there is no nest co-habitation by a male-female pair (Yunes et al., 1991). Lactating females display much more aggression towards sexually mature females than towards stranger or familiar males, and the presence of another female near the nest is deleterious for litter survival (Laconi, 1998; Laconi and Castro-Vázquez, 1998; Laconi et al., 2000). During the breeding period, females are territorial and their home ranges are both crossed by transient and by resident males but never by breeding females (Steinmann et al., 2008). On the other hand, males have home ranges that are twice as large as those of females and they fully share them with both sexes and their spatial distribution is strongly influenced by searching for mates (Steinmann et al., 2005, 2008). This spacing behaviour pattern of C. musculinus agrees with a promiscuous mating system (Steinmann et al., 2008). In promiscuous species, in which females typically mate with more than one male during each estrous period, males are expected to evolve large testes relative to their body size (Heske and Ostfeld, 1990). C. musculinus male's testis present an unusual development of Leydig cells, and testosterone levels in plasma higher than monogamous mouse and vole species (Castro-Vázquez et al., 1987; Buzzio and Castro-Vázquez, 2002). The age at which sexual maturation is reached, fecundity and the duration of breeding season are the most important reproductive variables in the determination of rodent population abundances (Dapson, 1979; Mihok et al., 1985; Rodd and Boonstra, 1988). In rodent populations the sexual maturation of juvenile cohorts can be related to the presence of adult animals (Wasser and Barash, 1983; Wolff et al., 2001; Wolff et al., 2002). Thus, the removal of specific segments of rodent populations affects reproduction in younger cohorts (Saitoh, 1981; Gilbert et al., 1986; Rodd and Boonstra, 1988; Pusenius and Viitala, 1993). In promiscuous species, territorial females are generally assumed to have a greater impact on inhibiting juveniles than males, due to the fact that females typically compete for exclusive offspring-rearing space (Wolff, 1993; Bond and Wolff, 1999). Thus, young females that cannot acquire an exclusive breeding site may delay sexual maturation until space becomes available (Wolff, 1997). Delayed sexual maturation or reproductive suppression of juveniles may result from either direct contact with adults generally through their intrasexual intolerant behaviour, or from chemical signals from urine of related or grouped females (Getz et al., 1983; Heise and Rozenfeld, 1999). However, Wolff et al. (2001) did not observe that the presence of mothers suppressed reproduction in their daughters for Microtus ochrogaster and M. pennsylvanicus. Besides, in Calomys venustus (a promiscuous-polygynous South American rodent) Priotto et al. (2006) observed that both juvenile females and males matured in relation to physiological times independently of the presence of adults. The aim of this study was to test the hypothesis that the presence of parents causes a delay in maturation and reproductive activity of spring-born females in fenced populations of C. musculinus, at the beginning of the breeding period.


This study was carried out on Espinal Reservation of the campus of the National University of Río Cuarto (33º 07S, 64º 14W). The study area was a natural pasture interspersed with bushy and weedy species, and it had high vegetal cover (about 100% throughout the year) being similar to natural habitats of C. musculinus. We set up four 0.25 ha enclosures (two control and two experimental) made of galvanized iron sheets extending 0.3 m underground and 0.7 m above ground. In each enclosure, six reproductive shelters were enclosed with a concrete circle of 1 m diameter and 0.7 m height and were covered by iron mesh. On the inner margin of each enclosure, a 1 m-wide grass strip was devegetated with herbicide. For a detailed description of the study area and enclosure construction see Priotto and Polop (2003), and Priotto et al. (2004). The study was carried out between September 2003 and February 2005. It had two periods: 1) Absence of fathers (AF) (from September 2003 to January 2004), and 2) Absence of mothers (AM) (from October 2004 to February 2005). Between AF and AM periods (February-September 2004) all animals captured in the enclosures were removed. The rodent populations were from an area located 30 km away from the place of study. In September and October 2003 (AF), and October and November 2004 (AM), 24 and 16 mates respectively were preserved in the laboratory in individual reproductive cages. In both periods, adults and their offspring were weighed and ear-tagged for permanent identification. Both, sex and birth date of the offspring were also recorded. In both periods, after the offspring were weaned in the laboratory, adults and their offspring were carried to the enclosures and then each family group was located in a reproductive shelter. After three days the reproductive shelters were opened and the animals dispersed into the enclosures. During AF period, in control enclosures both parents remained with the offspring (12 mates and 58 juveniles). In experimental enclosures only the adult females remained with their offspring (12 adult females and 45 juveniles). In AM period, there were 8 positive mating less than in AF period. In control enclosures both parents remained with their offspring (8 mates and 47 juveniles) whereas, in experimental enclosures only the adult males remained with their offspring (8 adult males and 49 juveniles). In each enclosure there was a CMR grid of 6 x 10 traps with an interstation interval of 6 m. One Sherman live-trap was placed at each station and baited with a mixture of peanut butter and cow fat. Three trapping sessions of 8 successive nights every fortnight were carried out from November to January in AF and from December to February in AM. In each devegetated edge, in order to detect those voles that were not able to settle in the habitat area of the plot, 28 Sherman live traps were placed at 6 m intervals. Animals that were trapped three consecutive times in devegetated edge areas within each trapping sessions were removed from the population since we assumed that they were not able to settle within the enclosures. Traps were checked each morning and trapped animals were weighed, and sex and reproductive state were recorded. New animals were individually marked with a numerical code in their ears and released in the site of capture. Reproductive condition of spring-born females was judged from vagina perforation (perforate or imperforate vagina), pregnancy and size of nipples. When reproductive condition of female could not be judged by external characters, the condition of vaginal smears was analysed. Vaginal smears were taken with a small Pasteur pipette and then a smear was made on a glass slide and observed under a microscope. Vaginal smears were classified as estrous smears when the number of cornified cells was greater than epithelial cells and leucocytes (Buzzio and Castro-Vazquez, 2002). Spring-born females were classified as immature if they had imperforate vagina or no estrous vaginal smear, mature but non-active if they had an estrous vaginal smear or perforate vagina but non-evidence of pregnancy or suckling, or mature and active if they were pregnant or suckling. 041b061a72


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