Early-summer inhibition of reproduction in wild white-footed mice (Peromyscus leucopus noveboracensis): influence of supplemental food

Adults of wild white-footed mouse (Peromyscus leucopus noveboracensis) populations in southeastern Virginia have been shown to be reproductively suppressed during May–July compared with other months of the reproductive season. The gonads and sex accessory glands are also significantly smaller during May–July than at other times of the year. The causes of this early summer reproductive suppression are unknown. In this study, food (Agway 3000) that could not be hoarded was supplied in feeding stations on one-half the 11-ha wooded study area during 1990 and 1991. Food consumption (g) was positively but not significantly correlated with population density (adults/ha) during both years. Population density was higher during 1991 on the food-supplemented area than on the nonsupplemented area, but the statistical significance was marginal. Mice of both sexes living on both areas during 1990 and 1991 exhibited significant reproductive suppression during May–June. Further, mice of both sexes living on both areas during both years had significantly smaller gonads and sex accessory glands during May–June compared with other months of the year. Thus, during both years, surplus food did not prevent suppression of reproductive function in this wild population, and this phenomenon remains unexplained. Received: November 4, 1998 / Accepted: October 5, 1999     

Vasopressin and aggression in cross-fostered California mice (Peromyscus californicus) and white-footed mice (Peromyscus leucopus)

To examine how developmental experiences alter neural pathways associated with adult social behavior, we cross-fostered pups between the more aggressive and monogamous California mouse (Peromyscus californicus) and the less aggressive and polygamous white-footed mouse (P. leucopus). Cross-fostered males became more like their foster parents when tested as adults. Male white-footed mice became more aggressive only in an aggression test in a neutral arena, whereas the territorial California mice became less aggressive in resident-intruder aggression test, as measured by attack latency. Only the species that displayed a change in resident-intruder aggression showed a change in arginine vasopressin (AVP) levels: cross-fostered California mice had significantly lower levels of AVP-immunoreactive (AVP-ir) staining than controls in the bed nucleus of the stria terminalis (BNST) and the supraoptic nucleus (SON) and a nonsignificant trend toward lower levels in the medial amygdala (MA). Neither species showed changes in AVP-ir staining in a control area, the paraventricular nucleus (PVN). The changes in AVP-ir staining in the BNST and SON may not be caused by stress because cross-fostering was not associated with changes in adult plasma concentrations of two steroid hormones, corticosterone and testosterone, that have been associated with stress-related alterations in AVP pathways. These results suggest that manipulating the early parental environment can directly alter both a neurotransmitter system and species-typical patterns of social behavior, but that these effects may vary between species and under different social contexts.     

Frequent Harderian gland adenocarcinomas in inbred white-footed mice (Peromyscus leucopus)

In 1997, three lines of inbred Peromyscus leucopus--GS109A, GS16A1, and GS16B--were acquired by the Peromyscus Genetic Stock Center. Since then, records have been kept on tumors detected by visible inspection of live animals. The inbred lines GS109A and GS16A1 presented tumors with frequencies substantially higher than that of the other inbred line or of random-bred P. leucopus stock. The average age of detection was 456 +/- 75 days (n = 24) for GS109A and 568 +/- 168 days (n = 12) for GS16A1 respectively. Surprisingly, the majority of the tumors (23 of 24 for GS109A and 8 of 12 for GS16A1) appeared to be Harderian gland lesions. During the same time period only a single tumor, a fibrosarcoma, was noted in the other inbred strain (GS16B), and one Harderian gland tumor was detected in the random bred stock. On the basis of the number of animals born to each group, tumor frequencies were approximately 22.7%, 8.3%, 0.67%, and 0.07%, for GS109A, GS16A1, GS16B, and randombred P. leucopus stock, respectively. The periocular tumors appeared to be highly malignant, with elevated mitotic indices, marked anaplasia, and metastases to regional lymph nodes and lungs. The tumors were readily transplantable to other animals of the same line. Among various other species, malignant Harderian gland tumors are relatively rare.     

Effects of heavy metals on immunocompetence of white-footed mice (Peromyscus leucopus)

Continued human population growth and industrialization result in increased contamination of wildlife habitats. Effects of such habitat deterioration on the well-being of natural populations are unclear. Exposure to contaminants may impair immunocompetence, thereby increasing disease susceptibility. The mammalian immune system is important in maintaining health and in its sensitivity to toxins. In our study conducted from May 1999 through May 2001, we examined assays of immnnoompetence in the white-footed mouse (Peromyscus leucopus) that inhabited reference sites and sites significantly contaminated with mixtures of heavy metals. We estimated potential exposure and uptake of heavy metals by measuring the level of each contaminant in representative soil and tissue samples. Intraindividual variation across mice, but not sex, explained a large portion of the overall variance in immune response, and spleen weight was significanltly afflicted by mouse age. We found no evidence that residence on contaminated sites had any effect on immunopathology and humoral immunity as measured in our study. We suggest that field and laboratory studies in ecotoxicology provide estimates of exposure to contaminants (i.e., tissue analyses) to establish a database suitable to clarify the dose-response relationship between contaminants and target systems.     

Dichlorvos toxicity in the white-footed mouse (Peromyscus leucopus)

The organophosphate pesticide, dichlorvos (DDVP), is used commonly to control ectoparasites in laboratory rodents colonies. This compound is relatively nontoxic to Mus musculus at dosages several times the therapeutic level. However, usage of a similar therapeutic level in the white-footed mouse (Peromyscus leucopus) resulted in substantial mortality. To determine whether P. leucopus is more susceptible than M. musculus to the toxic effects of DDVP, both species were exposed to 0, 3 and 6 g of pelleted DDVP per cage. In a subsequent experiment, P. leucopus were exposed to 0 and 1 g of DDVP per cage. Mortality was not observed in M. musculus at any dosage level. P. leucopus exposed to 1, 3 and 6 g of DDVP exhibited mortalities of 3%, 20% and 53%, respectively. Mean serum cholinesterase in P. leucopus exposed to 3 and 6 g of DDVP was 0.35 and 0.21 U/ml as compared to 3.13 U/ml in unexposed mice. The analogous values for M. musculus were 1.60 and 0.79 U/ml while the level in unexposed mice was 6.79 U/ml. In the second experiment, mean serum cholinesterase in P. leucopus exposed to 1 g of DDVP was 0.32 U/ml as compared to 2.33 U/ml in unexposed mice. Histopathology revealed no lesions in the brain, liver or kidneys. The increased susceptibility of P. leucopus to the toxic effects of DDVP was related to the lowered serum cholinesterase. This indicates that DDVP should not be used for control of ectoparasites in P. leucopus.     

Bone loss is a physiological cost of reproduction in white-footed mice (Peromyscus leucopus)

Investment in offspring production often requires the mobilization of endogenous resources, a strategy that may negatively impact maternal condition. In mammals, skeletal ossification in growing offspring requires a large investment of calcium by mothers, and bone loss has been described in several species as a means of supporting this demand. Although bone loss can have adverse effects on the mother, its potential role in a reproductive trade-off has not been addressed. Using white-footed mice (Peromyscus leucopus), we tested the effect of dietary calcium availability on maternal skeletal condition during reproduction to assess if calcium availability drives a trade-off between maternal skeletal condition and offspring production. We provided mice with a low-calcium or standard diet and monitored reproductive output along with changes in bone mineral density and bone resorption (via serum concentrations of pyridinoline cross-links) throughout reproduction. Reproductive performance was not impaired by low calcium intake. Reproductive females on the low-calcium diet showed a significant reduction in bone mineral density relative to reproductive females consuming the standard diet and non-reproductive mice consuming the low-calcium diet, but no difference in bone resorptive activity. Our results suggest that when dietary calcium is limited white-footed mice reproduce at the expense of their skeletal condition, and may do so by limiting bone mineral accretion relative to resorption.     

Effects of forest edge on populations of white-footed mice Peromyscus leucopus

Several studies have reported higher densities of white-footed mice in small fragments than in large fragments of eastern deciduous forests. The edge hypothesis states that higher densities in smaller fragments reflect an increase in relative amount of edge habitat, which supports higher densities of mice because of its higher quality. To test this hypothesis we live trapped white-footed mice along edge-to-interior gradients in forest fragments of east-central Illinois. Our results indicated a greater abundance of mice in the forest interior than near the edge, which did not support the edge hypothesis. This pattern could occur because dominant adults hold larger territories of higher quality habitat, thereby reducing density and increasing fitness near the edge (an ideal despotic distribution). We found some evidence of increased reproductive success (juveniles per female) at the edge, but this could reflect density-dependent demographic processes rather than habitat quality. Furthermore, other indicators of dominance (body weight, and reproductive activity) did not show an increase at the edge, and other studies indicate higher prevalence of natural enemies at edges, which could account for lower densities there. Reduced competition from larger rodents and reduced predation could cause higher densities in small fragments but the distributions of competitors and predators do not strongly support these hypotheses. We suggest two additional hypotheses that could account for greater densities in smaller fragments: 1) estimates of high densities could be artifacts of the large effect that a few captures can have on density estimates for very small fragments, and 2) densities in smaller fragments are overestimated because mice use a relatively larger area of surrounding habitat as fragment size decreases.     

Stimulus selection (light) in four subspecies of deermice (Peromyscus maniculatus)

Abstract

Four subspecies of deermice (Peromyscus maniculatus) were selected from habitats along a gradient from mesic hardwood forests (gracilis), tall grass prairie (bairdi), short grass prairie (nebrascensis), to desert grassland (labecula) in effort to relate the light preferences of the mice to the habitat of their origin. Six individuals of each subspecies were maintained in dark chambers for 25 days, during which they could turn on a dim light for 30 seconds on ten of these days. Mice from the mesic habitats turned the lights on more frequently (light reinforcement) than mice from xeric habitats. The same subspecies that exhibited light reinforcement when raised in laboratory light conditions failed to show light reinforcement when raised in total darkness. The circadian periodicities also differed significantly among the subspecies. Conclusions drawn from the results were: (1) selection for light is genetically influenced as indicated by subspecific differences, (2) some genotypes are readily modified by environmental light conditions than others, and (3) natural selection in each environment appears to contribute to the degree of genetic fixation or genetic plasticity.     

Effects of grouping and fighting on the reproductive tracts of male white-footed mice (Peromyscus leucopus)

Summary Adult, male white-footed mice (Peromyscus leucopus) were subjected to a variety of social situations ranging from isolation during the 20 day experimental period to constant contact with both females and other adult males. Contacts included grouping (three or four males per cage) and exposure to fighters (once daily for 20 minutes). The following measurements were recorded: weights of the body, testes, epididymides, vesicular glands, vesicular gland tissue (wet and dry), seminal fluid of the vesicular gland, adrenal glands, and baculum; spermatozoan reserves of the testes and epididymides. Grouping significantly affected both the weight and spermatozoan reserves of the testes and epididymides, as well as both the tissue and seminal fluid weight of the vesicular glands. The results suggested a graded effect of all treatments on the reproductive tract. In order of magnitude of the associated response, from none to greatest, the treatments may be ranked as follows: pairing with females, isolating, handling, fighting, and grouping. All reproductive parameters measured showed this general ranking, suggesting that the response to the various treatments was similar and differed only quantitatively. The results further suggested decreased secretion of LH and testosterone, although measurements of testosterone did not substantiate this conclusion. The lack of significant effects of grouping on adrenal gland weights strengthened the argument that adrenal involvement is not a necessary adjunct to the suppression of the reproductive tract in groupedPeromyscus, but the adrenal may be involved if contacts between males result in overt fighting.     

A possible mechanism of rapid luteolysis in white-footed mice,Peromyscus leucopus

Adult female white-footed mice, Peromyscus leucopus, were exposed to long (LP) or short (SP) photoperiods for 6 weeks (experiment I). Another group of animals was kept for 6 weeks in SP, then injected SC with 30 μg prolactin twice daily for 2, 3, 4, or 6 days (experiment II). Ovaries from the mice in both experiments were weighed and serially sectioned for light microscopic examination of regressing corpora lutea. In experiment I, it was observed that vessels supporting corpora lutea were dilated, and that their endothelium was either undergoing necrosis or it was missing. Pronounced changes of luteal capillaries led to rupture and intraluteal hemorrhage, thus opening the capillary bed. Regressing luteal cells became segregated and seemed to invade the vascular system passively. They were seen as luteal cell thrombi in medullary veins. This luteolytic course termed “rapid luteolysis” was most apparent in SP ovaries. It differed from “retarded luteolysis,” which represents the well-established luteolytic model of auto- and heterophagocytosis. In experiment II, there was a statistically significant decrease in ovarian weight 4 days after prolactin treatment in comparison with saline-treated controls. At the light microscopic level, signs of both rapid and retarded luteolysis were present, but not intensified. It is concluded: (1) The concept of rapid luteolysis represents a reasonable working hypothesis. (2) Prolactin, though luteolytic at the macroscopic level, failed to produce evidence of increased rapid or retarded luteolysis at the light microscopic level.     

Social environment modulates photoperiodic immune and reproductive responses in adult male white-footed mice (Peromyscus leucopus)

Social cues may interact with photoperiod to regulate seasonal adaptations in photoperiod-responsive rodents. Specifically, photoperiod-induced adjustments (e.g., reproduction and immune function) may differ among individuals in heterosexual pairs, same-sex pairs, or isolation. Heterosexual cues may be more influential, based on their potential fitness value, than same-sex cues or no social cues. The present study examined the effects of pair (with a male or female) or individual housing on reproductive and immune responses in male white-footed mice (Peromyscus leucopus) maintained in long or short photoperiods. Female pairing did not affect reproductive responses in short-day males. In long days, however, the presence of a female increased both testosterone concentrations and testes mass compared with individually housed and male-paired mice, respectively. Short-day, individually housed males enhanced delayed-type hypersensitivity (DTH) responses compared with single-housed mice in long days, but all paired groups decreased DTH responses regardless of photoperiod. The lack of enhanced DTH response in male mice paired with females coincided with reduced circulating corticosterone concentrations in both photoperiod treatments. Together, these results suggest that social environment may have important modulatory effects on photoperiod-regulated immune responses in male white-footed mice.     

Testicular apoptosis is down-regulated during spontaneous recrudescence in white-footed mice (Peromyscus leucopus).

Among individuals of many nontropical species, seasonal breeding is timed by tracking changes in the daily photoperiod. Transfer of rodents to short (< 12 h of light/day) day lengths for 6 to 14 weeks can induce regression of the testes mediated by apoptosis. After 16 to 20 weeks of short day exposure, reproductive function is "spontaneously" initiated, and testicular recrudescence is observed. The gonadal mechanisms that underlie testicular recrudescence are not fully understood. If the onset of testicular regrowth that occurs during spontaneous recrudescence reflects a down-regulation of apoptotic signals, then a decline in apoptosis should be noted concurrent with increased testis mass. This experiment sought to assess the role of apoptosis in the restoration of reproductive capacity to photoperiod-inhibited white-footed mice. Males were assigned to long (16:8 LD) or short (8:16 LD) photoperiods for 0, 14, 18, 22, 26, or 30 weeks. At each of these time points, testis mass and testosterone concentrations were assessed. In addition, apoptotic activity was measured using both in situ terminal deoxynucleotidyl transferase dNTP end labeling (TUNEL) and DNA laddering. Short photoperiod exposure induced maximal decreases in testicular parameters after 14 weeks (p < 0.05). After 26 weeks of short days, testis mass was no longer different between males housed in long days and those housed in short days. In contrast, the high incidence of apoptotic TUNEL labeling and DNA laddering observed at 14 weeks was reduced to long day values after 22 weeks of short day exposure. Together, our results establish that a decrease in testicular apoptosis coincides with testicular recrudescence in white-footed mice. The current study demonstrates a decline in the incidence of testicular cell death concomitant with changes in testis mass or length, elucidating a timeline of changes at the cellular level related to the onset of recrudescence.     

Borrelia burgdorferi infection in white-footed mice (Peromyscus leucopus) in hemlock (Tsuga canadensis) habitat in western Pennsylvania.

White-footed mice (Peromyscus leucopus) were captured and their tissues sampled from 27 sites in seven counties of western Pennsylvania in 1990 for isolation and identification of Borrelia burgdorferi. Two hundred sixty mice were captured from which there were 27 isolations. Significantly more mice were captured and significantly more isolations made from hemlock (Tsuga canadensis) habitat than from deciduous species forest. Hemlock habitat is sparse and focal but evidently increases winter survival of mice, and thus possibly results in increased infection rates in mice.     

Number of immunoreactive GnRH-containing neurons is heritable in a wild-derived population of white-footed mice (Peromyscus leucopus)

The evolution of mammalian brain function depends in part on levels of natural, heritable variation in numbers, location, and function of neurons. However, the nature and amount of natural genetic variation in neural traits and their physiological link to variation in function or evolutionary change are unknown. We estimated the level of within-population heritable variation in the number of gonadotropin-releasing hormone (GnRH) neurons, which play a major role in reproductive regulation, in an unselected outbred population recently derived (<10 generations) from a single natural population of white-footed mice (Peromyscus leucopus, Rafinesque). Young adult male mice exhibited an approximately threefold variation in the number of neurons immunoreactive for GnRH in the brain areas surveyed, as detected using SMI-41 antibody with a single-label avidin-biotin complex method. Consistent with earlier findings of selectable variation in GnRH neurons in this population, the level of genetic variation in this neuronal trait within this single population was high, with broadsense heritability using full-sib analysis estimated at 0.72 (P<0.05). Either weak selection on this trait or environmental variation that results in inconsistent selection on this trait might allow a high level of variation in this population.     

Immune response, not immune maintenance, is energetically costly in wild white-footed mice (Peromyscus leucopus)

Understanding the cost of immune function is essential for more accurate characterization of energy budgets of animals and better understanding of the role of immunity in the evolution of life-history strategies. We examined the energetic cost of maintaining a normally functioning immune system and mounting a mild immune response in wild male white-footed mice (Peromyscus leucopus). To evaluate the cost of maintaining immunocompetence, we compared resting and daily metabolic rates (RMR; DMR) and masses of body organs of mice whose immune systems were suppressed by cyclophosphamide with those of control mice. To evaluate the cost of mounting an immune response, we measured RMR, DMR, and organ masses in mice whose humoral and cell-mediated immune responses had been stimulated by injections of sheep red blood cells and phytohemagglutinin, respectively. Immunosuppression resulted in a significant reduction in circulating leukocytes, by 225%, but no significant effect on metabolic rates or organ masses. Immunochallenged animals showed no significant differences in metabolic rates compared with control animals but did exhibit significantly smaller dry masses of the small intestine and testes, by 74% and 22%, respectively. We concluded that the cost of maintaining the immune system was minimal. In contrast, there was a significant energetic cost of mounting an immune response that, depending on its magnitude, can be met through reductions in energy allocation to other physiological systems.     

Recovery of reproductive function by prairie deermice (Peromyscus maniculatus bairdii) from asymptotic populations

Prairie deermice greater than 100 days of age and non-reproductive in laboratory populations provided with surplus food and water were paired either with fertile mates or with other inhibited population animals. Following pairing, more than 75 per cent of all animals reproduced. The rates of reproductive recovery did not differ significantly between males and females. The average time required for reproduction by population animals paired with proven mates was less than that for pairs composed of population animals. The significantly slower rate of reproductive recovery for population pairs suggests that mutual stimulation is involved in recovery and is initially lacking or minimal in these pairs. A period of physiological and behavioural adjustment following removal from the populations appears necessary before reproduction. Mechanisms preventing reproduction within the populations are unknown.