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Population parameters of Peromyscus leucopus (white-footed deermice) inhabiting a heavy metal contaminated superfund site.

Tar Creek Superfund Site, located in extreme northeastern Oklahoma, contains multiple lead and zinc mines dating from the early 1900s that operated until deposits were depleted in the 1970s (United States Environmental Protection Agency, 2005). During this time, sulfide forms of lead and zinc and, to a lesser extent, zinc carbonate, lead carbonate, and lead phosphate were mined, resulting in extraction of ca. 1.7 million metric tons of lead ore and 8.8 million metric tons of zinc ore (United States Fish and Wildlife Service, 2000). Much of the preliminary processing of ore, or smelting, occurred locally (Gibson, 1972). Both mining and smelting produced numerous sources of contamination, particularly milled mine waste, flotation tailings, and aerial particulates, all of which contain residual heavy metals, including lead, zinc, and cadmium (Datin and Cates, 2002; Agency for Toxic Substances and Disease Registry, 2004). About 75 million metric tonnes of crushed mine tailings are deposited in large mounds scattered throughout the site and sediment retention ponds cover ca. 325 ha (United States Environmental Protection Agency, 2005). In addition to obvious destruction of terrestrial habitats, acidic drainage from mines contaminated Tar Creek and the surrounding watershed and wetlands (United States Fish and Wildlife Service, 2000). Because of concerns regarding exposure to heavy metals, the United Stated Environmental Protection Agency listed the 65-[km.sup.2] area on the National Priorities List in 1983 (United States Environmental Protection Agency, 2005). Numerous studies have documented exposure to heavy metal contaminants by human residents within Tar Creek Superfund Site (Lynch et al., 2000; Malcoe et al., 2002; Agency for Toxic Substances and Disease Registry, 2004); however, no study has documented impacts on other mammalian species, with the exception of Odocoileus virginianus (white-tailed deer; Conder and Lanno, 1999).

A plethora of endpoints exist that can be used to determine exposure and effects of environmental contamination on different organisms. These may include individual-based measurements of biochemical, physiological, behavioral, and morphological endpoints or measurements of endpoints including perturbations at population and community levels (Kendall et al., 2001). Although there are innovative laboratory techniques used for predicting effects on natural populations, there are few in situ field studies illustrating effects of contaminants, either directly or indirectly, on wild mammalian populations (Flickinger and Nichols, 1990; Linzey and Grant, 1994; Klosinska, 1996; Allen and Otis, 1998; Block et al., 1999; Boonstra and Bowman, 2003).

Small mammals, particularly rodents, are a valuable resource for determining effects of exposure to contaminants (Rowley et al., 1983; Talmage and Walton, 1991; Linzey and Grant, 1994), with a range of detrimental effects resulting from chronic exposure to heavy metals being reported (Kisseberth et al., 1984; Ma, 1989; Shore and Douben, 1994). Small mammals are useful indicator species because they have relatively small home ranges allowing a direct tie to the source of contamination, they have a generalized diet, they represent an important food source for predators, their short life spans allowing examination of successive generations, and they occupy habitats that increase exposure through ingestion and inhalation of contaminated soils (Jenkins, 1981; Talmage and Walton, 1991). Moreover, Peromyscus leucopus (white-footed deermice) are ubiquitous throughout much of North America, often occurring at relatively high densities, and can be captured easily. Peromyscus leucopus has been used extensively as an indicator species in environments contaminated with heavy metals (McBee and Bickham, 1990; Smith et al., 2002).

A variety of different molecular, cellular, physiological, and behavioral biomarkers have been used successfully with small mammals for determining effects of exposure to contaminants (McBee and Bickham, 1990; Talmage and Walton, 1991; Peakall and McBee, 2001). Such assays provide valuable information regarding mechanisms of action and dose-response relationships between contaminants and characteristics of small mammals. However, effects at the population level, which can provide ecologically relevant information about species under natural environmental conditions, have rarely been studied or reported, particularly in the case of contamination by heavy metals (Sheffield et al., 2001).

The objective of this study was to test the hypothesis that ecological characteristics of populations of P. leucopus from Tar Creek Superfund Site would be significantly altered compared to reference populations from uncontaminated sites. Specifically, we hypothesized that there would be smaller population sizes, reduced rates of survival and reproductive activity, and disproportionate sex ratios and age structure at contaminated sites within Tar Creek Superfund Site compared to uncontaminated reference sites. Additionally, we hypothesized that individuals of populations inhabiting contaminated sites would exhibit increased incidence of abnormal dental characteristics and increased rates of ectoparasitic infestation, indicating compromised overall health.

Materials and Methods--Communities of small mammals were sampled at two locations within Tar Creek Superfund Site and two uncontaminated reference sites, Lake Carl Blackwell and Oologah Wildlife Management Area. Sites within Tar Creek Superfund Site, a desiccated sediment-retention pond (hereafter Douthat) and an abandoned mining site (hereafter Beaver Creek), were chosen based on current and historical evidence of contamination by heavy metals (United States Environmental Protection Agency, 2000, 2005). Both sites were located in Ottawa County, Oklahoma, and were ca. 7.5 km apart. Due to the immense size of Tar Creek Superfund Site, reference sites had to be located outside of the immediate area to prevent the possibility of aerial and hydrologic transport of contaminants. Lake Carl Blackwell, Payne County, Oklahoma, and Oologah Wildlife Management Area, Nowata County, Oklahoma, were chosen as reference sites because of general vegetative and topographic similarities to both contaminated sites, as well as proximity to contaminated sites. All sites comprised equal areas of mixed-grass prairie and cross-timber habitats, and had similar vegetational structure (Phelps, 2006; Phelps and McBee, 2009).

Each site was sampled seasonally during June 2004-March 2006. Sherman live traps (H. B. Sherman Traps, Inc., Tallahassee, Florida), baited with rolled oats, were placed on a 10 by 10 permanent grid with 10-m spacing. Traps were baited during late afternoon and checked early the following morning for 4 consecutive days, equaling 400 trap-nights/trapping session (100 traps times 4 nights). Our sampling protocol consisted of 8 primary sampling sessions each consisting of 4 consecutive days of trapping (secondary trapping sessions). This sampling scheme follows the robust design used to achieve maximum efficiency in estimating size of population and rate of survival from markrecapture data (Pollock et al., 1990).

Location of trap, species, age, sex, reproductive status (males were classified as scrotal or non-scrotal, females were classified as pregnant, lactating, post-lactating, or non-breeding), body mass, dental condition, presence and location of external parasites, and overall body condition were recorded for all captured individuals. Lastly, individuals were marked with a unique identification number by toe clipping, and then released at site of capture (Twigg, 1975). All procedures were conducted following standards set forth by the Animal Care and Use Committee of the American Society of Mammalogists and under Oklahoma State University Animal Care and Use Protocol AS056.

Following the robust design (Pollock et al., 1990), trapping data from secondary trapping sessions were used to estimate size of populations of P. leucopus using the index, [M.sub.t+1] (Otis et al., 1978). This is a closed-population estimator and assumes that there is no mortality and no immigration or emigration during each 4-day trapping session. Estimates of size of populations were analyzed using two-way analysis of variance, with time (i.e., trapping session) being considered a repeated measure, to determine if there were differences in average size of populations of P. leucopus among sites and seasons (PROC GLM; SAS Institute, Inc., 2000).

Mark-recapture data from primary trapping sessions were used to determine rates of survival ([PHI]) and recapture ([rho]) using the Cormack-Jolly-Seber open-population model in program MARK (White and Burnham, 1999). Four assumptions must be met for the Cormack-Jolly-Seber model to fit the data correctly: 1) every marked individual that is present in the population immediately after i has the same probability of survival until the next sampling period, i + 1; 2) every individual present at the time of the ith sample has an equal probability of capture; 3) marks cannot be lost or overlooked; and 4) all samples are instantaneous and all individuals are released immediately after capture (Pollock et al., 1990). Assumptions 1 and 2 were tested using program MARK and our sampling protocol allowed for assumptions 3 and 4 to be met. A global model was constructed within program MARK that included effects of group (site), time (trapping session), and interactions on rates of survival and recapture. Goodness-of-fit test using RELEASE (version 3.0, embedded in program MARK) was performed to determine if data were overdispersed; i.e., to determine if enough explanatory factors were included in the model to explain the variation. To account for overdispersion, likelihoods of models were divided by an overdispersion factor and used to adjust future models accordingly. To determine the best model for our data, 16 predefined models in program MARK were run and the most appropriate model was selected based on an information-theoretic criterion, Akaike's Information Criterion (AIC). The most-parsimonious model is one that yields the lowest QAIC value (Pryde, 2003). Mean minimum longevity was calculated for each site by averaging the time, in months, between the first and last capture of each individual that was captured during [greater than or equal to] 2 trapping sessions.

A female was considered reproductively active if signs of pregnancy (distended abdomen with palpable fetuses) or enlarged nipples were present. Relative frequency of reproductively active female P. leucopus was compared among sites using a Chi-square test (PROC FREQ SAS Institute, Inc., 2000). Additionally, an index of reproductive success was computed as the number of juveniles per number of adult females captured during a trapping session, and effects of site and season were compared using two-way analysis of variance (PROC GLM; SAS Institute, Inc., 2000).

Assuming equal probability of capture between sexes, overall sex ratios were generated by pooling all trapping sessions and relative numbers of males and females were compared among sites for departures from an expected 1:1 ratio using a Chi-square test (PROC FREQ; SAS Institute, Inc., 2000). Age structure was determined by pooling trapping sessions, and relative number of adults and juveniles were compared among sites to determine if patterns in distribution of captured individuals within age classes were similar among sites using a Chi-square test (PROC FREQ; SAS Institute, Inc., 2000). Differences in average body mass of adult, non-reproductive individuals were compared among sexes and sites using two-way analysis of variance (PROC MIXED; SAS Institute, Inc., 2000). For individuals captured on multiple occasions, a single capture was randomly chosen for inclusion in the above analyses.

Dental condition was assessed by inspecting upper and lower incisors, noting any departures from normal coloration of enamel, which is typically yellow-orange and glossy, presence of dental lesions, such as chipped or broken teeth, or both. Individuals were placed into categories as described by Boulton et al. (1999): 1, normal; 2, slight mottling; 3, extensive mottling; 4, completely whitened; or 5, fractured or broken. Data for sexes and trapping sessions were pooled and a Chi-square test was used to determine differences in number of individuals by categories of dental condition (i.e., 1-5) among sites (PROC GLM; SAS Institute, Inc., 2000).

Although numerous ectoparasites are known to infest P. leucopus, within our study, only larvae of botflies could be counted accurately. No attempt was made to rear adult botflies from the infesting larvae; however, Cuterebra fontinella is a species that typically infests P. leucopus throughout the midwestern states (Clark and Durden, 2002; Barko, 2003). Incidence of parasitism by botflies (number of parasites for each infected host) and prevalence (number of parasitized individuals per total number of captured individuals) were compared among sites using one-way analysis of variance (PROC GLM; SAS Institute, Inc., 2000).

If the interaction variable in two-way analysis of variance was not significant, main effects were examined and considered significant if P [less than or equal to] 0.05. Additionally, post hoc contrasts between reference sites, Lake Carl Blackwell and Oologah Wildlife Management Area combined, and contaminated sites, Douthat and Beaver Creek combined, were conducted.

Results--Sites were sampled for 12,800 trap-nights (3,200 trap-nights/site), during which 10 species of small mammals were captured (Peromyscus leucopus, P. maniculatus, Sigmodon hispidus, Neotoma floridana, Reithrodontomys fulvescens, R montanus, Microtus pinetorum, M. ochrogaster, Blarina hylophaga, and Mus musculus). Peromyscus leucopus was the most frequently captured species at all sites with the exception of Oologah Wildlife Management Area, where P. leucopus was second to S. hispidus (hispid cotton rat). In fact, P. leucopus comprised a substantial proportion of total captures at both contaminated sites (ca. 60%) compared to Lake Carl Blackwell and Oologah Wildlife Management Area (45.5 and 31.6%, respectively). A total of 271 P. leucopus was captured during the 2-year sampling period (Lake Carl Blackwell, n = 62; Oologah Wildlife Management Area, n = 81; Douthat, n = 81; Beaver Creek, n = 47). Of 271 unique individuals captured, 215 were recaptured at least once during the study (Lake Carl Blackwell, n = 44; Oologah Wildlife Management Area, n = 67; Douthat, n = 61; Beaver Creek, n = 41). Mean number of individuals captured at Lake Carl Blackwell across all trapping sessions was 10.5 [+ or -] 5.8, Oologah Wildlife Management Area 17.3 [+ or -] 6.3, Douthat 15.1 [+ or -] 8.1, and Beaver Creek 10.3 [+ or -] 4.6. Estimates of size of populations were based on total captures during each trapping session and were assumed to be an equal proportion of the actual population present at each site. Sizes of populations were not significantly different among sites ([F.sub.3, 16] = 2.39, P = 0.11) or seasons ([F.sub.3, 16] = 1.81, P = 0.19), with no site-by-season interaction ([F.sub.9, 16] = 0.68, P = 0.72; Fig. 1).

A goodness-of-fit test to assess the assumption of equal probabilities of survival (assumption 1) was not significant ([[chi square].sub.28] = 9.44, P = 0.99), indicating that individuals from all sites had an equal probability of surviving to the next trapping session regardless of being marked previously. Similarly, the assumption of homogeneity of captures (assumption 2) was not significant ([[chi square].sub.15] = 22.91, P = 0.09), indicating that individuals from all sites had an equal probability of capture.

We selected a model, based on the lowest QAIC value, in which rates of survival varied by time (trapping session) and rates of recapture varied by group (site). Rates of survival were lowest during December 2004-March 2005 (0.44 [+ or -] 0.08) followed closely by March 2005-June 2005 (0.45 [+ or -] 0.08; Table 1). Rates of recapture were highest at both contaminated sites, Douthat and Beaver Creek, (0.63 [+ or -] 0.10) and lowest at Lake Carl Blackwell (0.38 [+ or -] 0.09; Table 2). A significant difference in mean minimum longevity was observed among sites ([F.sub.3, 95] = 2.85, P = 0.04). Peromyscus leucopus inhabiting Oologah Wildlife Management Area and Beaver Creek (6.75 and 6.00 months, respectively) had significantly greater mean minimum longevity than counterparts inhabiting Lake Carl Blackwell and Douthat (4.60 and 4.89 months, respectively).

Relative frequency of reproductively active females was not significantly different among sites ([[chi square].sub.3] = 7.26, P = 0.06); however, Lake Carl Blackwell had the highest percentage of reproductive females of the total population of females (48.4%), followed by Douthat (31.4%). Oologah Wildlife Management Area and Beaver Creek had similar percentages of reproductive females, 23 and 20%, respectively. Reproductive success was not significantly different among sites ([F.sub.3, 16] = 1.88, P = 0.17) or seasons ([F.sub.3, 16] = 2.58, P = 0.09), with no significant site-by-season interaction ([F.sub.9,16] = 1.16, P = 0.20).

Sex ratios did not differ significantly among sites ([[chi square].sub.3] = 2.29, P = 0.52). The ratio of adults to juveniles, or age structure, was significantly less disproportionate at Douthat (1:0.53) compared to Beaver Creek (1:0.18) and both reference sites, Lake Carl Blackwell and Oologah Wildlife Management Area, (1:0.22 and 1:0.27, respectively; [[chi square].sub.3] = 8.94, P = 0.03; Table 3). Body mass of non-reproductive adults was significantly different among sites ([F.sub.3, 267] = 5.48, P < 0.01) and between sexes ([F.sub.1, 267] = 13.59, P < 0.01).

[FIGURE 1 OMITTED]

There was no site-by-sex interaction ([F.sub.3, 267] = 1.3, P = 0.28; Table 3). Beaver Creek had significantly larger non-reproductive adults compared to Lake Carl Blackwell (t = 3.89, P < 0.01); however, there was no other significant difference among sites. Comparison of combined reference sites to combined contaminated sites yielded a significant difference in average body mass of non-reproductive adults (post hoc contrast: [F.sub.1, 267] = 12.04, P < 0.01), with contaminated sites having a larger average body mass than reference sites.

Individuals from reference sites were scored for two categories of dental condition (1 and 2); whereas, contaminated sites had individuals placed into three of the five categories (1, 2, and 3). There was a significant difference in relative frequency of individuals from each site in each category ([[chi square].sub.6] = 53.75, P < 0.01; Fig. 2), indicating a higher proportion of individuals with abnormal dental characteristics were captured at contaminated sites compared to reference sites. Additionally, neither reference site had individuals exhibiting extensive mottling of upper and lower incisors (i.e., category 3).

A bimodal seasonal pattern of parasitism by botflies was observed, with most individuals (96%) being parasitized by one or more botflies during summer and winter trapping sessions with no evidence of parasitism observed during trapping sessions in spring and autumn. Only one exception occurred: two individuals from Beaver Creek trapped during September 2005 each had one botfly present. Prevalence of infestation (number of individuals infested with a botfly divided by number of individuals captured) was highest at Oologah Wildlife Management Area (23.46%) and lowest at Lake Carl Blackwell (6.56%), with Douthat and Beaver Creek being intermediate (19.75 and 12.50%, respectively). A significant difference in prevalence was observed among sites ([F.sub.3, 267] = 2.83, P = 0.04), with a greater prevalence of infested individuals occurring at Oologah Wildlife Management Area compared to Lake Carl Blackwell (t = 2.70, P = 0.03). Incidence of infestation by botflies ranged from an average of 1 botfly/infested host at both Lake Carl Blackwell and Beaver Creek to 1.15/host at Oologah Wildlife Management Area and 1.28/host at Douthat; however, incidence of infestation was not significantly different among sites ([F.sub.3, 44] = 0.73, P = 0.54).

Discussion--Because data were too sparse to use computer programs MARK and CAPTURE, estimates of size of populations were based on number of individuals captured during each trapping session for each site. We avoided using the minimum-number-known-alive formula, an open-population estimator that violates Pollock's robust design (Pollock et al., 1990). Although size of populations of P. leucopus were not significantly different among sites, some sites, specifically Douthat and Oologah Wildlife Management Area, exhibited wide fluctuations during the 2-years of this study (Fig. 1). For example, between trapping sessions in December 2004 and June 2005, size of the population inhabiting Douthat decreased >50%; whereas, during this same time, size of the population of P. leucopus at Oologah Wildlife Management Area increased by 142% then decreased by 48% until December 2005. Fluctuations in populations of small mammals are common (Linzey and Kesner, 1991; Allen and Otis, 1998); however, the genus Peromyscus exhibits characteristically less variation in size of populations than some other species of small mammals, such as Microtus pennsylvanicus (meadow vole) and Reithrodontomys megalotis (western harvest mouse; Lackey et al., 1985).

We determined that individuals from all sites had equal probabilities of surviving from one trapping session to the next regardless of being marked previously (assumption 1 in Cormack-Jolly-Seber model); therefore, we selected a model in which rates of survival for individuals residing at each site were grouped to determine rates of survival among trapping sessions. Rates of survival varied among trapping sessions, but the difference was not significant (Table 1). With all sites combined, survival was lowest between December 2004 and March 2005, which corresponds to reduction in size of populations at both contaminated sites, Douthat and Beaver Creek (Fig. 1). Conversely, populations at both reference sites, Lake Carl Blackwell and Oologah Wildlife Management Area, increased between December 2004 and March 2005. This trend of decreasing size of populations at contaminated sites and increasing size of populations at reference sites continued between the next trapping sessions, March 2005 and June 2005. The time between March 2005 and June 2005 also had the second lowest rate of survival between trapping sessions during this study (Table 1). Interestingly, rates of survival for P. leucopus tend to be highest during winter and lowest during spring and summer (Lackey et al., 1985). All sites were sampled within a time frame of ca. 2 weeks to minimize effects of differing weather conditions; therefore, climatic effects cannot explain the contrast in trends of populations between reference and contaminated sites. Probabilities of recapture were not significantly different among sites, indicating that individuals inhabiting each site had equal probability of being recaptured after initial capture (assumption 2 in Cormack-Jolly-Seber model); however, both contaminated sites had higher rates of recapture than either reference site (Table 2). Logically, if a site has a high rate of recapture of individuals, then these individuals must be residing within the area for extended periods of time. Perhaps, populations of P. leucopus on contaminated sites are composed predominately of resident individuals, whereas individuals on reference sites may be more transient. However, mean minimum longevity values, or amount of time an individual resides on a trapping grid, were not significantly different among contaminated and reference sites.

[FIGURE 2 OMITTED]

Fluctuations in populations of small mammals can be attributed to changes in reproductive parameters, such as proportion of reproductively active females and reproductive success (Terman, 1968). Linzey (1987) reported that significantly fewer offspring survived from litters of pairs of P. leucopus exposed to PCBs in the laboratory, but numerous field studies reported that reproductive characteristics of populations of small mammals residing on contaminated sites were similar to those of reference populations (Linzey and Grant, 1994; Klosinska, 1996; Block et al., 1999; Boonstra and Bowman, 2003). Proportion of reproductively active females was not significantly different among our sites, nor was reproductive success. Allen and Otis (1998) speculated that their observation of a positive correlation between concentrations of dieldrin in substrates and number of female Peromyscus maniculatus (North American deermice) exhibiting signs of reproductive activity was confounded by higher rates of capture of reproductively active females on contaminated sites because higher demand for energy was driving them to search for food in unfamiliar places, such as traps. We were unable to determine if reproductively active females foraged more actively or widely on contaminated sites than on reference sites.

Wild populations of P. leucopus typically exhibit a male-biased sex ratio, largely because males tend to travel over greater distances; therefore, they have a higher probability of exposure to traps (Terman, 1968). Kaufman and Kaufman (1982) reported that sex ratios were slightly skewed toward more males; however, sex ratios were similar to a 1:1 ratio in Kansas. Most of our sites, with the exception of Douthat, exhibited female-biased sex ratios, which may be explained by reduced recruitment of males into the population or differential trapability between males and females due to differences in movement patterns, behavioral response, environmental factors, etc. Age structure can reveal the level of recruitment of adults into the population; however, disproportionate age structure may result due to the lower success in capturing juveniles. The proportion of juveniles within the population at Douthat was nearly double that of all other sites. Linzey and Grant (1994) reported a higher proportion of juvenile and subadult P. leucopus inhabiting a PCB-contaminated grid compared to a reference grid, hypothesizing that the PCB-contaminated grid was serving as a sink for subordinate individuals inhabiting higher quality habitats nearby. A significantly greater percentage of juveniles and subadults compared to adult P. leucopus were reported inhabiting herbicide-treated pastures compared to untreated reference pastures (McMurry et al., 1996).

Physical condition of exposed individuals can provide insight into acclimation undertaken to cope with residing in a disturbed habitat. Body mass may be positively or negatively correlated with exposure depending on the contaminant (Rowley et al., 1983; Linzey, 1987; McMurry, 1993; Boonstra and Bowman, 2003). Boonstra and Bowman (2003) reported that male Blarina brevicauda (northern short-tailed shrew) inhabiting a grid contaminated with high levels of PCBs had significantly greater average body mass compared to individuals from grids with lower levels of contamination. Klosinska (1996) examines two possible reasons for an increase in body mass, particularly associated with an increase in fat reserves, both related to disturbance in normal metabolic functioning. Heavy metals are not easily eliminated through normal metabolic processes and may be sequestered in liver, kidney, and bone tissue, in addition to fat, where they become physically inert. Circulation of lead within the body also can inactivate enzymes essential to lipid metabolism, resulting in greater fat reserves and ultimately greater total body mass (Klosinska, 1996). We detected that adult, non-reproductive P. leucopus inhabiting contaminated sites had significantly greater average body mass than those within reference sites (Table 3); however, mechanisms associated with this discovery are unknown.

All calcified tissues, such as teeth and bones, can incorporate heavy metals into their mineral phase during development (Appleton et al., 2000; Gdula-Argasinska et al., 2004). Appleton et al. (2000) reported that concentrations of heavy metals were significantly higher in teeth of Myodes glareolus (bank vole) residing within industrial sites in southern Poland compared to reference sites. Furthermore, Appleton et al. (2000) concluded that teeth accurately serve as indicators of exposure to contamination by heavy metals. However, increased concentrations of heavy metals in dental tissues have not been correlated with altered color or texture in small mammals. Abnormal dental conditions in S. hispidus have been noted in studies examining exposure to petrochemical wastes, particularly fluoride (Rafferty et al., 2000; Kim et al., 2001). Both Rafferty et al. (2000) and Kim et al. (2001) reported relatively few dental abnormalities in S. hispidus collected from reference sites; however, nearly one-half of all examined individuals from petrochemical waste sites exhibited some departure from normal dental coloration, texture, or both. In addition, presence of dental abnormalities was correlated strongly to concentrations of fluoride in bone and soil (Rafferty et al., 2000). Within our study, nearly all individuals residing within Lake Carl Blackwell and Oologah Wildlife Management Area exhibited normal dental coloration and texture (98.4 and 95.6%, respectively) and only a small portion exhibited slight departures (1.6 and 7.4%, respectively; Fig. 2). Nearly one-half of all captured individuals at Douthat and Beaver Creek exhibited normal dental characteristics (55.0 and 66.7%, respectively), nearly one-third of captured individuals were placed in category 2 (41.3 and 31.3%, respectively), and incidences of extensive mottling (category 3) were noted only for individuals captured at contaminated sites (3.8 and 2.1%, respectively; Fig. 2).

In conclusion, we observed higher rates of recapture at contaminated sites compared to reference sites; in addition, incidences of extensive dental mottling were only noted for individuals residing on contaminated sites. At contaminated sites, particularly Beaver Creek, individuals, on average, had larger body masses compared to individuals inhabiting reference sites. Interestingly, individuals from Douthat exhibited trends for some characteristics that were incongruent with all other sites. Within Douthat, there was a disproportionate number of juveniles and sex ratio was male-biased. Although we were not able to determine levels of contaminants within biological tissues in our study, Moeller (2004) reported that substrates from Douthat had levels of cadmium, zinc, and lead that were ca. 180, 210, and 23% higher, respectively, than those at Beaver Creek, indicating that Douthat is a more heavily contaminated environment than Beaver Creek. This evidence may explain these incongruent results. While past mining practices may be influencing some ecological characteristics of populations of P. leucopus within Tar Creek Superfund Site, we cannot determine if direct or indirect effects of residual heavy metals present throughout the site or the extensive habitat disturbance caused these alterations. In fact, most basic demographic parameters of this commonly captured species were not measurably different among contaminated and reference sites, contrary to what we hypothesized. Perhaps, this may indicate that characteristics of short-lived, omnivorous species, such as P. leucopus, are not sensitive to contamination by heavy metals or that responses at the population level are not detectable unless they greatly exceed natural variation in populations; therefore, these are not useful indicators of environmental exposure to hazardous mining waste present within Tar Creek Superfund Site. Further study is needed to elucidate subtle relationships among chronic exposure to heavy metals, disturbance of habitat resulting from past mining practices, and characteristics of populations of P. leucopus at Tar Creek Superfund Site.

We thank the Quapaw Tribe of Oklahoma, United States Corps of Engineers, and Oklahoma State University for access to study sites; numerous field technicians, particularly S. J. Smith, K. A. Hays, J. S. Newcomb, A. Carroll, and Z. P. Henson; M. E. Payton and W. D. Warde for statistical assistance; S. F. Fox and J. R. Bidwell for editorial assistance; J. C. Diaz for translation of the abstract into Spanish; and Sigma Xi and Oklahoma State University Zoology Graduate Student Society for funding.

Submitted 30 January 2008. Accepted 14 October 2009.

Editor was Michael L. Kennedy.

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KENDRA L. PHELPS * AND KAREN MCBEE

Department of Zoology and Collection of Vertebrates, Oklahoma State University, Stillwater, OK 74078

Present address of KLP: Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409

* Correspondent: kendra.phelps@ttu.edu
Table 1--Quarterly estimates of survival ([PHI]) for populations of
Peromyscus leucopus (white-footed deermice) from uncontaminated
reference sites, Lake Carl Blackwell and Oologah Wildlife Management
Area, and from two sites within Tar Creek Superfund Site, Douthat and
Beaver Creek. The most-parsimonious model produced using program MARK
indicated that rates of survival varied by time (trapping session).

Time                            [PHI]      SE        95% CI

June 2004-September 2004        0.822    0.123    0.472-0.960
September 2004-December 2004    0.724    0.123    0.426-0.903
December 2004-March 2005        0.440    0.085    0.286-0.607
March 2005-June 2005            0.454    0.081    0.305-0.611
June 2005-September 2005        0.722    0.101    0.491-0.873
September 2005-December 2005    0.590    0.111    0.370-0.779
December 2005-March 2006        0.596    0.151    0.302-0.834

TABLE 2--Estimates of probability ([rho]) of recapture for populations
of Peromyscus leucopus (white-footed deermice) from uncontaminated
reference sites, Lake Carl Blackwell and Oologah Wildlife Management
Area, and from two sites within Tar Creek Superfund Site, Douthat and
Beaver Creek. The most-parsimonious model produced using program MARK
indicated that rates of recapture varied by group (site).

Group                                [rho]      SE        95% CI

Lake Carl Blackwell                  0.380    0.092    0.222-0.467
Oologah Wildlife Management Area     0.592    0.081    0.429-0.737
Douthat                              0.631    0.106    0.412-0.806
Beaver Creek                         0.635    0.100    0.427-0.802

TABLE 3--Comparison of sex ratios, percentage of adults and juveniles,
and average body mass (mean [+ or -] SE)of adult, non-reproductive
Peromyscus leucopus (white-footed deermice) captured on uncontaminated
reference sites, Lake Carl Blackwell and Oologah Wildlife Management
Area, and from two sites within Tar Creek Superfund Site, Douthat and
Beaver Creek. Values were obtained after pooling all trapping sessions.
Size of sample is included in parentheses.

                        Sex ratio      Percentage    Percentage
Site                  (male:female)    of adults    of juveniles

Lake Carl Blackwell   1:1.0 (31:31)    82.3 (51)      17.7 (11)
Oologah Wildlife
  Management Area     1:1.2 (37:44)    79.0 (64)      21.0 (17)
Douthat               1:0.8 (46:35)    65.4 (53)      34.6 (28)
Beaver Creek          1:1.1 (22:25)    85.4 (40)      14.6 (7)

                                     Average body mass (g)

Site                           Males                    Females

Lake Carl Blackwell   21.2 [+ or -] 0.8 (31)    19.7 [+ or -] 1.1 (30)
Oologah Wildlife
  Management Area     23.3 [+ or -] 0.6 (36)    20.2 [+ or -] 0.5 (44)
Douthat               22.9 [+ or -] 0.7 (46)    22.3 [+ or -] 1.0 (34)
Beaver Creek          25.7 [+ or -] 0.7 (22)    22.2 [+ or -] 0.6 (24)
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Author:Phelps, Kendra L.; McBee, Karen
Publication:Southwestern Naturalist
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Geographic Code:1USA
Date:Sep 1, 2010
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