
==== Front
Environ Sci Pollut Res Int
Environ Sci Pollut Res Int
Environmental Science and Pollution Research International
0944-1344
1614-7499
Springer Berlin Heidelberg Berlin/Heidelberg

39150665
34667
10.1007/s11356-024-34667-y
Research Article
Pronounced declines in heavy metal burdens of Minnesotan mammals over the last century
http://orcid.org/0000-0002-2972-5895
Snell-Rood Emilie C. emilies@umn.edu

Kjaer Savannah J.
Marek-Spartz Mary
Devitz Amy-Charlotte
Jansa Sharon A.
https://ror.org/017zqws13 grid.17635.36 0000 0004 1936 8657 Department Ecology, Evolution and Behavior, University of Minnesota, Twin Cities, 1479 Gortner Ave, Gortner 140, St Paul, MN 55108 USA
Responsible Editor: Wei Liu

16 8 2024
16 8 2024
2024
31 39 5247352484
21 2 2024
5 8 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Humans have drastically altered the ecology of heavy metals, which can have negative effects on animal development and neural functioning. Many species have shown the ability to adapt to anthropogenic increases in metal pollution, but such evolutionary responses will depend on the extent of metal variation over space and time. For terrestrial vertebrates, it is unclear how metal exposure has changed over time: some studies suggest metal content peaked with the enactment of policies controlling lead emissions, while other studies suggest metal levels peaked at least a century earlier. We used 162 specimens of four mammal species (a mouse, shrew, bat, and squirrel) to ask how metal content of the fur and skin has changed over a 90-year time period, and impacts on individual performance (body size and cranial capacity). Using ICP-MS, we show that for lead, cadmium, copper, and chromium, there were significant declines in metal content in mammal tissue over the 90-year time period, with lead levels five times lower now than in the early 1900s. Importantly, metal content began to drop well before the pollution regulation of the 1970s. Effects of time greatly outweighed any effects of an individual living near a human population center. Surprisingly, there were no effects of body metal content on body size, and only manganese was negatively related to relative cranial capacity. Taken together, these results suggest that present day populations of mammals are experiencing levels of heavy metal exposure that are less stressful than they were 100 years ago. In addition, temporal decreases in metal loads likely partly reflect global patterns of pollution decline that affect atmospheric metal deposition rather than local point sources of exposure.

Supplementary Information

The online version contains supplementary material available at 10.1007/s11356-024-34667-y.

Keywords

Heavy metals
Pb
Ecotoxicology
Minnesota
Rodents
Bioaccumulation
http://dx.doi.org/10.13039/100000001 National Science Foundation DEB-2045382 Snell-Rood Emilie C. http://dx.doi.org/10.13039/100012149 Minnesota Environment and Natural Resources Trust Fund ML2022 CH 94 ART SEC 2 SUB 08E APPR 2022 Snell-Rood Emilie C. issue-copyright-statement© Springer-Verlag GmbH Germany, part of Springer Nature 2024
==== Body
pmcIntroduction

Heavy metals, such as lead, can be toxic in animal development, especially to the developing nervous system of vertebrates (Galiciolli et al. 2022; Green and Planchart 2018; Mason et al. 2014; Robards and Worsfold 1991). Humans have drastically changed how metals move through ecosystems, with mining and industrial practices moving metals from once inaccessible locations into terrestrial and aquatic environments where they often enter the food chain (Ali et al. 2019, Bindler et al. 2008; Fang et al. 2019; McConnell et al. 2018). As metal pollutants have increased in natural ecosystems, some species have evolved traits or strategies to cope (Hoostal et al. 2008; Janssens et al. 2009; Klerks and Weis 1987; Papadopulos et al. 2021), such as increases in the copy number of metal-processing genes in fungi dealing with metal industry (Bazzicalupo et al. 2020). Most studies considering adaptation to heavy metal pollution focus on plants, microbes, and invertebrates; it is less clear how vertebrates respond to metal pollution over long periods of time, and the corresponding implications for metals as potent neurotoxins.

In order to understand ecological and evolutionary responses to metal pollution, we need to first understand how patterns of heavy metal exposure have changed over time. In particular, when and where levels of metals are the highest should correspond to the greatest selection on metal tolerance. Many studies have shown that the metal content of animals and plants has been declining over the last several decades, especially for lead (Pb) (Chadwick et al. 2011; Helander et al. 2019; Jones et al. 1991; Lind et al. 2006; Nyholm and Rühling 2001). Much of this research has focused on the decades following lead removal from gasoline starting in the 1970s, and corresponding declines in body lead content of wild organisms (Chadwick et al. 2011; Helander et al. 2019; Jones et al. 1991; Lind et al. 2006; Nyholm and Rühling 2001) and humans (Egendorf et al. 2021; Han et al. 2018; Lacerda et al. 2023). A handful of studies have gone further back in time, but with conflicting results. Some ice core data from Arctic sites suggests the 1970s are indeed the peak of lead emissions (McConnell et al. 2019), and studies of marine invertebrates (sponges, corals, mollusks) with centuries-old skeletal remains further corroborate this finding (Asami et al. 2021; Gillikin et al. 2005; Jacobson 2023; Shen and Boyle 1987). However, ice and sediment core data from other locations suggests that lead emissions may have peaked much earlier (McConnell and Edwards 2008; McConnell et al. 2014). Indeed, lead from leaded gasoline account for less than 20% of excess lead globally (Farmer et al. 1996), and metal emissions from coal burning may have been a major driver of earlier pollutant levels (Gabrielli et al. 2020; McConnell and Edwards 2008). In addition, some long-term studies of soil lead suggest that the declines in lead over time are spatially idiosyncratic (Datko-Williams et al. 2014). We lack studies of long-term trends in vertebrate heavy metal content that are necessary to pinpoint the strongest windows of selection on metal tolerance.

In this work, we ask how heavy metal levels in terrestrial mammals have changed over a 94-year time span (1911–2005), and how such long-term patterns compare to spatial variation in metal exposure. The metal content of organisms is often elevated closer to cities (Nava-Diaz et al. 2015), and point sources of metal pollution (Berglund and Nyholm 2011), suggesting spatial variation in selection for metal tolerance. We focus on six heavy metals associated with human activity (lead, cadmium, zinc, copper, chromium, nickel, manganese), and ask whether these anthropogenic metal pollutants vary in concert with human activity (as in Gabrielli et al. 2020; Wiener and Sandheinrich 2010), or show distinct patterns over time and space (e.g., copper and zinc have increased over time, Polak-Juszczak 2013). While lead often receives much of the attention because it is tightly regulated, metals such as cadmium and manganese are receiving increasing attention as neurotoxins (Bakulski et al. 2020; Cecil 2022), and metals such as copper are sometimes even more toxic than lead for some species (Xin et al. 2015). We predicted that tissue lead content would decline precipitously following increased regulations in the 1970s (Chadwick et al. 2011; Helander et al. 2019; Jones et al. 1991; Lind et al. 2006; Nyholm and Rühling 2001), but that such declines started even earlier due to reduced atmospheric inputs (McConnell and Edwards 2008; McConnell et al. 2014). We predicted metals in general would be correlated as part of an anthropogenic “syndrome” of metals (Kaushal et al. 2020). We also predicted that metal content would generally be positively associated with human population density (over space), and that spatial variation would be as important as temporal variation. Understanding these patterns is essential in knowing predicting metal stress, and resulting selection on metal tolerance.

To sample animals broadly across space and time, we made use of natural history collections of mammals (as part of University of Minnesota’s Bell Museum of Natural History). Such collections allow additional tests of the effects of metals on phenotypes and are increasingly recognized as critical resources in studies of urban ecology and evolution (Shultz et al. 2021). If we assume that tissue metal content reflects something about environmental exposure, as seen in controlled rearing studies (Baker et al. 1998; Farag et al. 1994; Hollis et al. 2001), we can ask if individuals with higher metal burdens show phenotypic responses such as reduced body size or reduced relative brain size. Because many metals are neurotoxins, and exposure to metal pollution early in life is related to reductions in neural volume in human and rodent models (Buford et al. 2023; Cecil et al. 2008; Seo et al. 2023), we might predict that cranial volume is negatively correlated with body metal content for wild animals as well. In our previous work, we used external measurements of small mammal skulls (Elton et al. 2001; Finarelli 2006, 2011) from the Bell Museum’s collections to investigate how urbanization affects cranial volume (Snell-Rood and Wick 2013). Here, we return to those specimens and ask how body metal content varies with body size and relative cranial capacity.

Methods

Specimens and sample collection

We focused on a subset of specimens from the University of Minnesota’s Bell Museum of Natural History mammal collection that were measured in a previous study (Snell-Rood and Wick 2013). Specimens of adult individuals were chosen to span urban and rural populations over a 90-year time period. We captured data from specimen tags, including sex, date, and place of capture, as well as standard measurement data, including weight, total length from head to tail, tail length, hindfoot length, and ear length. We also took three measurements from the neurocranium to estimate cranial volume (see Snell-Rood and Wick 2013): length (nasal/frontal suture to the top of the foramen magnum), width (widest part of the parietal and squamosal bones), and height (the basisphenoid to the highest point on the top of the cranium) were used to estimate volume, as corroborated by existing studies (Elton et al. 2001; Finarelli 2006, 2011). We focused on four species that represents a range of diets, including a bat (Eptesicus fuscus, Palisot de Beauvois, 1796; N = 21 specimens), a shrew (Blarina brevicauda, Say, 1823, N = 71 specimens), a mouse (Peromyscus leucopus, Rafinesque, 1818, N = 45 specimens), and a squirrel (Sciurus carolinensis, Gmelin, 1788, N = 25 specimens).

Animals accumulate heavy metals differently across different tissues (and across metals, e.g., Mukhtar et al. 2020; Nardiello et al. 2019). Thus, we chose to standardize tissue collection and focus comparisons within each metal. From each sample, we cut an approximately 5 mm × 5 mm square piece of skin and fur from the belly of the animal, using stainless steel dissecting scissors. These samples weighed, on average, 5.95 mg. Due to limits on weighing specimens in the collections where we accessed them, five samples weighed below the target 1 mg of tissue we were aiming for, 0.4–0.98 mg), but were still above the limit of detection for our metals of interest.

Measurement of metal content

The metal content of each sample was measured using ICP-MS at the Northwestern University Quantitative Bio-element Imaging Center using their standard protocols. Briefly, samples were first digested with 250 μ l HNO3 and 50 μ l H2O2 in a 65-C water bath for 4 h until completely dissolved. To each sample, 4.7-mL Millipore H2O was added prior to running on the ICP-MS. We focused on seven metals: lead (Pb), cadmium (Cd), zinc (Zn), copper (Cu), chromium (Cr), manganese (Mn), and nickel (Ni). We chose these metals because they are of contaminant and health concern in the Twin Cities, and can all be measured with the same protocol. We additionally considered arsenic (As) as a contaminant of concern in the Twin Cities (Minneapolis and St Paul, MN, northcentral USA), but first assessed whether measure measures could be confounded with past preservation techniques that used arsenic (Found and Helwig 1992; Hawks and Williams 1986). Indeed, we found that arsenic levels in the samples were skewed towards very high levels for samples from 1945 and earlier, so we did not consider arsenic in the tests of our predictions. However, we do report the measured values here and in the supplemental text (Figure S1) as this subset of samples averaged 52,000 ppm arsenic (note that the lethal dose is humans is 140–1400 mg for an average sized adult).

Measures of spatial variation in human population centers

We were interested in the spatial context of each specimen in terms of adjacent human population and associated development. For each specimen, we first pulled latitude and longitude data from the Global Biodiversity Information Facility (gbif.org) for each georeferenced specimen. Because exact collection coordinates were available for only 80% of samples, our primary measure of human population density was the population density of the county of collection at the time of collection. We took data on the population size of the county at the closest date of the US Census relative to the collection date of the specimen and calculated human population density by dividing by the area of the county. To investigate if a spatially finer measure of population density mattered, for specimens with precise location data, we matched the collection date to the nearest census date for the town closest to the collection location. Specimens were on average 4700 m from the nearest population center. We used the human population size and distance to this population center to classify urban and rural categories. Analyses with this measure of urbanization did not qualitatively change the reported results, so we report findings at the county level, where we have data for all of our specimens.

Statistical analysis

All statistical analyses were run in JMP 17.0 (SAS Institute). In our first set of analyses, we were primarily interested in time, human population density, and species as independent variables, with tissue metal content as response variables. We predicted that the effects of time would vary with location and species, so we additionally included time–species and time–population density interactions in the model. In our second set of analyses, we were primarily interested in performance measures as the response variable (body size and relative brain size). We focused on time and species as the primary independent variables, and included time–species interactions. Relative cranial capacity was taken as the residuals from species-specific linear models that included body length and sex. We used body length, as opposed to weight, assuming that it was a more accurate measure of size as mass is influenced by current condition and hydration. When analyses were re-run with other morphological measures such as hindfoot length or tail length, they were qualitatively identical. Because a previous study on these specimens found effects of time and space on relative cranial capacity (Snell-Rood and Wick 2013), we included year of collection and human population density in analyses of cranial capacity and metal content. In all analyses, we used log-transformed values for metal content and body size measures to avoid several large values biasing the linear models. All data are archived in Snell-Rood et al. (2024).

Results

Time is the primary determinant of specimen metal content, not urbanization

First, we asked whether the heavy metal content of mammal tissue declined over time, and to what extent such declines varied with species, or human population density (as a measure of urbanization). We measured metal content of 171 specimens (of four species, see Fig. 1), spanning a 94-year time period, from 1911 to 2005 (median year of sampling = 1964). We measured the human impact of a population based on the population density of the county where the specimen was collected at the time point when it was collected (see methods).Fig. 1 Map of specimen collection locations relative to present-day human population density. Teal shading shows variation in (present day) human population density across the state of Minnesota (USA), shown as raw population counts for a given municipality. The collection locations of specimens used in the study are shown as shapes, with squares corresponding to the shrew (Blarina brevicauda, N = 71), triangles to the bat (Eptesicus fuscus, N = 21), circles to the mouse (Peromyscus leucopus, N = 45), and diamonds to the squirrel (Sciurus carolinensis, N = 25). Collection locations are indicated by the position of the shape, note that when exact coordinates were unknown, the midpoint of the county is indicated, which may in some cases result in overlap

The most important determinant of specimen metal content was the year the specimen was collected (Table 1). There were significant declines in metal content over time for lead (Pb), cadmium (Cd), copper (Cu), and chromium (Cr), with the strongest time effects for lead, and the lowest for chromium (Table 1, Fig. 2). Indeed, in considering the oldest specimens (1911–1931, N = 14), lead levels were five times higher (71.2 ppm) than the most recent specimens (14 ppm; 1999–2005, N = 14). Given the hypothesized importance of time, we also tested for significant interactions between time and urbanization, and time and species, finding no effects. Table 1 Effects of time, urbanization, and species on tissue metal content

Metal	Year	Species	Pop density	Year × pop	Year × species	
Pb	F1,152 = 33.8

P < 0.0001

bST =  − 0.01

	F3,152 = 12.40

P < 0.0001

E > P = B > S

	F1,152 = 0.15

P = 0.69

	F1,152 = 0.53

P = 0.47

	F3,152 = 0.92

P = 0.43

	
Cd	F1,152 = 20.7

P < 0.0001

bST =  − 0.01

	F3,152 = 8.31

P < 0.0001

E > P, S; B > S

	F1,152 = 0.04

P = 0.82

	F1,152 = 0.55

P = 0.46

	F3,152 = 2.03

P = 0.08

	
Zn	F1,152 = 0.15

P = 0.69

	F3,152 = 31.0

P < 0.0001

B > P,S; P,E > S

	F1,152 = 2.31

P = 0.13

	F1,152 = 0.07

P = 0.79

	F3,152 = 2.14

P = 0.09

	
Cu	F1,152 = 15.3

P < 0.0001

bST =  − 0.007

	F3,152 = 8.78

P < 0.0001

B = P = E > S

	F1,152 = 0.26

P = 0.62

	F1,152 = 0.28

P = 0.59

	F3,152 = 0.52

P = 0.67

	
Ni	F1,152 = 0.01

P = 0.95

	F3,152 = 1.04

P = 0.38

	F1,152 = 0.00

P = 0.99

	F1,152 = 0.12

P = 0.73

	F3,152 = 2.15

P = 0.10

	
Cr	F1,152 = 8.21

P < 0.001

bST =  − 0.005

	F3,152 = 13.0

P < 0.0001

E > B,S,P,B > S

	F1,152 = 0.29

P = 0.59

	F1,152 = 0.69

P = 0.40

	F3,152 = 0.22

P = 0.88

	
Mn	F1,152 = 1.19

P = 0.28

	F3,152 = 16.4

P < 0.0001

B = P = E > S

	F1,152 = 0.48

P = 0.48

	F1,152 = 2.81

P = 0.09

	F3,152 = 1.28

P = 0.28

	
Shown are the results of a general linear model for seven metals (log-transformed ppm), testing the effects of time (year specimen collected), county human population density (“Pop density” or “Pop”) at the time of collection (log transformed), species, and interactions with time. When the model detected a significant effect of species, a Tukey HSD test was used to determine differences between species (where E = Eptesicus fuscus, P = Peromyscus leucopus, B = Blarina brevicauda, and S = Sciurus carolinensis). All significant results of time are plotted in Fig. 2

Fig. 2 Variation in specimen metal content over time. The concentrations of four metals (lead = Pb, cadmium = Cd, copper = Cu, chromium = Cr) was primarily determined by the year a specimen was collected, across four species considered (bat silhouette, red line = Eptesicus fuscus, mouse silhouette, green line = Peromyscus leucopus, shrew silhouette, blue line = Blarina brevicauda, and squirrel silhouette, purple line = Sciurus carolinensis)

“Species” was a significant cause of variation in metal content for lead, cadmium, zinc, copper, and chromium. In general, the bat showed the highest levels of metals, and the squirrel the lowest (Table 1, Fig. 2). Zinc was an exception, where the shrew tended to show the highest levels, although not significantly greater than bats. Unexpectedly, there were few to no effects of human population density on specimen metal content (Table 1).

Morphology is generally not affected by metal exposure

Second, we asked how individual body size and cranial capacity were related to metal exposure, using tissue metal content as a proxy for earlier life metal exposure. We predicted that body size and relative cranial capacity would decrease with metal content. Unexpectedly, we found no evidence that individuals with higher body metal content were smaller in terms of body length (not including tail length, Table 2) for each of the metals considered. Analyses were qualitatively similar when using hindfoot as a measure of body size. In addition, there were no significant interactions between metal content and species, suggesting species showed similar reactions to increasing metal exposure. Table 2 Effects of tissue metal content on body length

Metal	Year	Species	Pop density	Metal	Metal × species	
Pb	F1,152 = 0.13

P = 0.72

	F3,152 = 387.4

P < 0.0001

	F1,152 = 0.58

P = 0.44

	F1,152 = 1.12

P = 0.29

	F3,152 = 1.03

P = 0.38

	
Cd	F1,152 = 0.28

P = 0.59

	F3,152 = 410.4

P < 0.0001

	F1,152 = 0.52

P = 0.47

	F1,152 = 0.01

P = 0.92

	F3,152 = 2.11

P = 0.10

	
Zn	F1,152 = 0.85

P = 0.36

	F3,152 = 90.8

P < 0.0001

	F1,152 = 0.42

P = 0.52

	F1,152 = 0.19

P = 0.66

	F3,152 = 0.55

P = 0.65

	
Cu	F1,152 = 0.16

P = 0.69

	F3,152 = 272.1

P < 0.0001

	F1,152 = 0.30

P = 0.59

	F1,152 = 0.71

P = 0.44

	F3,152 = 0.44

P = 0.72

	
Ni	F1,152 = 1.30

P = 0.26

	F3,152 = 591.6

P < 0.0001

	F1,152 = 0.46

P = 0.50

	F1,152 = 2.87

P = 0.09

	F3,152 = 0.19

P = 0.66

	
Cr	F1,152 = 0.64

P = 0.43

	F3,152 = 472.7

P < 0.0001

	F1,152 = 0.34

P = 0.56

	F1,152 = 0.21

P = 0.65

	F3,152 = 0.62

P = 0.43

	
Mn	F1,152 = 0.95

P = 0.33

	F3,152 = 269.9

P < 0.0001

	F1,152 = 0.40

P = 0.53

	F1,152 = 0.02

P = 0.89

	F3,152 = 1.68

P = 0.17

	
Shown are the results of a general linear model testing the effects of body metal content on body length (log-transformed), for each of seven metals (log-transformed). Each model controls for the effects of time (year specimen collected), and the population density of the county of collection at the time of collection (log-transformed), in addition to species. We were interested in whether the effects of each metal varied with species, and thus included the metal-by-species term

Given that several of these metals are neurotoxins, we next asked whether proxies for brain size, taken from three linear skull measures, were correlated with an individual’s metal content. Because skull cranial capacity varies with body size and sex, we fist calculated “residual cranial capacity” from species-specific models that included body length and sex. There were no metals with consistent negative effects on relative cranial capacity across species (Table 3). However, the effects of manganese varied with species, showing significant negative effects in mice and significant positive effects in bats (Table 4, Fig. 3). Table 3 Effects of tissue metal content on relative cranial capacity

Metal	Year	Pop density	Species	Metal	Metal × species	
Pb	F1,141 = 0.46

P = 0.50

	F1,141 = 3.33

P = 0.07

	F3,141 = 0.21

P = 0.89

	F1,141 = 0.13

P = 0.71

	F1,141 = 0.13

P = 0.93

	
Cd	F1,141 = 1.44

P = 0.23

	F1,141 = 3.85

P = 0.05

	F3,141 = 29

P = 0.84

	F1,141 = 0.13

P = 0.72

	F1,141 = 0.53

P = 0.66

	
Zn	F1,141 = 1.34

P = 0.25

	F1,141 = 3.73

P = 0.06

	F3,141 = 0.08

P = 0.97

	F1,141 = 0.00

P = 0.95

	F1,141 = 0.86

P = 0.36

	
Cu	F1,141 = 1.60

P = 0.21

	F1,141 = 3.76

P = 0.05

	F3,141 = 0.18

P = 0.91

	F1,141 = 0.04

P = 0.84

	F1,141 = 0.11

P = 0.95

	
Ni	F1,141 = 1.11

P = 0.29

	F1,141 = 3.33

P = 0.07

	F3,141 = 0.13

P = 0.94

	F1,141 = 3.44

P = 0.07

	F1,141 = 0.44

P = 0.73

	
Cr	F1,141 = 2.09

P = 0.15

	F1,141 = 3.41

P = 0.07

	F3,141 = 0.18

P = 0.91

	F1,141 = 0.82

P = 0.37

	F1,141 = 0.15

P = 0.93

	
Mn	F1,141 = 2.18

P = 0.14

	F1,141 = 4.70

P = 0.03

	F3,141 = 0.77

P = 0.51

	F1,141 = 0.14

P = 0.71

	F1,141 = 4.42

P = 0.005

	
Shown are the results of a general linear model testing the effects of body metal content on cranial capacity. Cranial capacity is measured as the residuals from a model controlling for body length and sex, run individually for each species. The effects of seven metals were tested separately, with each model controlling for the effects of time (year specimen collected), and species. We were interested in whether the effects of each metal varied with species, and thus included the metal-by-species term

Table 4 Effects of manganese on cranial capacity across species

Species	Year	Population density	Log(Mn)	
Blarina brevicauda	F1,60 = 2.85

P = 0.10

	F1,60 = 1.38

P = 0.25

	F1,60 = 0.54

P = 0.47

	
Estesicus fuscus	F1,16 = 8.48

P = 0.01

bST = 0.001

	F1,16 = 1.93

P = 0.18

	F1,16 = 15.2

P = 0.001

bST = 0.039

	
Peromyscus leucopus	F1,41 = 0.39

P = 0.53

	F1,41 = 6.42

P = 0.02

	F1,41 = 10.4

P = 0.003

bST = -0.033

	
Sciurus carolinensis	F1,18 = 0.17

P = 0.69

	F1,18 = 18

P = 0.68

	F1,18 = 0.29

P = 0.59

	
Shown are the results of general linear models testing the effects of body manganese content on cranial capacity for each species (given the species-metal interaction reported in Table 3)

Fig. 3 Cranial capacity varies with manganese exposure across species. Shown are plots of relative cranial capacity (residuals of species-specific regressions for body length and sex on cranial capacity). All statistics are shown in Table 4 (bat silhouette = Eptesicus fuscus, mouse silhouette = Peromyscus leucopus, shrew silhouette = Blarina brevicauda, and squirrel silhouette = Sciurus carolinensis)

Discussion

Time as a primary determinant of metal content

In this research, time was the primary determinant of metal content across four species of mammals and five metals. These temporal trends are in line with studies finding declines in body lead content since the 1970s (Chadwick et al. 2011; Helander et al. 2019; Jones et al. 1991; Lind et al. 2006; Nyholm and Rühling 2001), but extend this work by showing that the declines started much before policy interventions in the 1970s (Fig. 2). A handful of studies on marine invertebrates that extend back at least 100 years show that animal body lead content peaked in the 1970s (Gillikin et al. 2005; Jacobson 2023; Shen and Boyle 1987) in contrast to the present study. It is possible that the different inputs of lead pollution affect marine and terrestrial ecosystems differently, or there is enough spatial variation in deposition that temporal peaks of metal pollution are variable over species and geography (e.g., Qian et al. 2023).

The observed declines over the last 100-year period, without spatial effects of human population density, are more consistent with atmospheric deposition through general air pollution rather than urban point sources of metal pollution. Indeed, collection studies of birds over the last 135 years show a dramatic decline in black carbon deposited on feathers as the air quality shifted with changes in coal burning (Dubay and Fuldner 2017). Given the link between coal burning, atmospheric metal deposition, and accumulation in vertebrate tissue in even remote areas (Kålås et al. 2000), our results are consistent with temporal shifts in overall air pollution exposing mammals to heavy metals. It is also possible that other wide-ranging changes in pollution could have driven the patterns seen here. For instance, global declines in acid rain could cause declines in metal bioavailability (Scheuhammer 1991). More fine-scale measures of metal speciation or stable isotope states could clarify these hypotheses for the underlying cause of the observed patterns.

This work assumes that metal accumulation in mammal skin and fur reflects variation in metal exposure earlier in life. An alternate explanation is that accumulation of metals in tissue varies with tolerance. Indeed, evidence from plants suggests that more tolerant populations raised in high metal conditions accumulate less metals in their tissue (Boquete et al. 2021; Meerts and Van Isacker 1997). Thus, a population adapting to high metals could show a decline in metal levels over time due to increased tolerance and genetic change in metal accumulation. However, it is unclear whether such physiological abilities apply to animals, which tend to accumulate metals in their tissue with exposure (Baker et al. 1998; Farag et al. 1994; Hollis et al. 2001). In addition, our results are consistent with the declines in atmospheric metals over the observed time periods (McConnell and Edwards 2008; McConnell et al. 2014). This work also assumes that our measures of fur and skin represent tissue accumulation of metals, rather than external deposition; future efforts that compared washed and unwashed skin could provide clarity (Ellis et al. 2023).

The lack of spatial effects in our analyses could potentially stem from an incomplete measure of human sources of pollution. We assumed that measures of human population density would be correlated with metal inputs through traffic volume, fuel burning, and urban industry. However, there are important point sources of pollution in more sparsely populated areas such as the mining region of northeastern Minnesota where acidic mine tailings can leach metals into the environment (Baeten 2018). Only one of our samples came from this region, and levels of lead (and iron) in this sample were average. It is also possible that our county-level measure of human population density was too coarse of a measure. For a subset of samples, we had more fine-scale measures of population density (Figure S2), but none of the effects of time changes when this measure is used in models. The only change with respect to spatial variation in human population density was the appearance of a significant interaction between time and space for cadmium (Table S1), where cadmium decreases over time in samples only in the urban-collected specimens (Figure S3). Thus, it is possible that declines in cadmium are being driven by different factors than the other metals. With respect to measures of spatial variation in pollution, it is possible that measures such as impervious surface area could be more appropriate.

Species differences as a secondary determinant of metal content

Metal content varied significantly across the four mammal species in the study. Much of this variation likely stems from variation in diet, which affects biomagnification of metals across trophic levels. All four of our study species occupy unique dietary niches, albeit with some degree of overlap. The big brown bat (E. fuscus) represents the highest trophic position, with a purely insectivorous diet that is dominated by hard-bodied beetles and moths, although with some seasonal variation (Agosta and Morton 2003; Swier 2003). Across the metals we considered, the bat tended to have the highest levels, especially for lead, cadmium, and chromium (Table 1). The short-tailed shrew (B. brevicauda) also has a relatively high trophic position, primarily feeding on invertebrates (isopods, beetles, and earthworms), but it also scavenges and preys on small mammals, including voles and mice (Babcock 1914; Shull 1907). Indeed, the shrew had the highest levels of zinc and copper (Table 1). The white-footed mouse (P. leucopus) exhibits significant seasonal and spatial variation in their diet, feeding on a variety of seeds, cultivated crops (i.e., corn, soy), and invertebrates depending on what is available (Whitaker 1966, Wolff 1985). Accordingly, the mouse samples were generally in the middle for all of the metals measured (Table 1). Finally, the gray squirrel (S. carolinensis) has the most plant-dominated diet, consuming seasonally available nuts, seeds, buds, and fruits, with only a small fraction of their diet represented by invertebrates (Nixon et al. 1968). Thus, not surprisingly, the squirrel had the lowest metal burdens (Table 1, Fig. 1).

Our findings are consistent with previous studies of metal accumulation in these species. Previous work comparing the trophic transfer of mercury in B. brevicauda and P. leucopus demonstrated that the shrews’ predominantly insectivorous diet resulted in much greater accumulation of mercury in the kidneys compared to the more omnivorous mice (Talmage and Walton 1993). Invertebrates, especially species like earthworms and beetles, can be important vectors for metal transfer to higher trophic levels (Goldsmith and Scanlon 1977; van Straalen and van Wensem 1986). Interestingly, there is debate in the literature as to whether lead tends to biomagnify across trophic levels with some studies finding evidence of biomagnification (e.g., Rubio-Franchini and Rico-Martínez 2011), and others finding none (e.g., Cardwell et al. 2013). Our results support the possibility of lead biomagnification, with bats showing the highest lead levels and squirrels the lowest (Table 1). It is possible that the chemical form of lead in the ecosystem could explain variation across studies as it has been reported that in inorganic forms (e.g., derived from leaded paint versus tetraethyl lead in fuel), lead does not tend to biomagnify (Eisler 1988).

Metals generally were not negatively related to body size or cranial capacity

Unexpectedly, we found no negative effects of body metal content on body size (Table 2), and no negative effects of lead, cadmium, copper, zinc, or nickel on relative cranial capacity (Table 3). Given the known neurotoxic effects of these metals (Buford et al. 2023; Cecil et al. 2008; Seo et al. 2023), especially lead, these findings were surprising. It is possible that the relatively lower levels of these metals in recent decades, compared to higher levels in the late 1800s, mean that current exposure has few toxic effects relative to the past. It is also possible that external skull measurements are too crude to capture more subtle neurotoxic effects of these metals. We used three linear measures of the skull to estimate cranial capacity; while past studies have validated these measures (Elton et al. 2001; Finarelli 2006, 2011), three dimensional CT scans would be a much more accurate representation of brain size, and would also delineate different brain regions that could be differentially impacted by metal exposure (Sakai et al. 2011; Witmer et al. 2008). Finally, it is possible that that our measures of tissue lead, from adult skin and fur lead content, poorly capture levels of metal exposure during early development of these species. Ideally, we would want a signature of metal exposure during brain development. However, metal concentration of the epidermis can decrease over time if an animal moves to an area of lower metal concentration as metals are shed through molting and developmental turnover (e.g., Dauwe et al. 2003; Honda et al. 1986; Hyvärinen et al. 2003). Using bone or teeth as focal tissues could potentially be better proxies of early life lead exposure due to patterns of lead uptake in juveniles and low rates of bone turnover in adults (Oflaherty 1995; Gullson and Gillings 1997).

We did see negative effects of body manganese content on relative cranial capacity in mice. This is consistent with evidence in the medical literature of this metal as an important neurotoxin (Balachandran et al. 2020; Dobson et al. 2004; O’Neal and Zheng 2015; Pfalzer and Bowman 2017) and suggests more research is needed in an ecological context. Oddly, there was a positive correlation between manganese and relative cranial capacity in bats, which could possibly be an artifact of selection on cranial capacity in this species (see Snell-Rood and Wick 2013) and correlated changes in exposure to the metal (rather than a causal relationship). Manganese is an important micronutrient in neural function (Pfalzer and Bowman 2017; Tuschl et al. 2013), but the levels we observed in tissues (average = 21 ppm in bat tissue), relative to requirements in mammals (0.028 ppm intake daily in humans), suggest it is not limited in availability. It is also possible that we could see species- and element-specific variation in patterns as metals vary in their ability to cross the blood–brain barrier, and in how they do so (Karri et al. 2016; Yokel 2006); thus, variation across species in neural physiology (e.g., cell transporters and concentrations of elements like calcium) could result in variation across species in effects on brain development (e.g., Fig. 3). Either way, this work points to manganese as a metal that deserves more attention in the literature.

Conclusions and implications

This study used mammals from a 100-year time span to ask how heavy metal exposure varied over time and space. Most of the heavy metals considered showed significant declines over the last 100 years, starting earlier than the 1970s lead regulations. There were no effects of human population density. These findings are consistent with studies implicating wide ranging deposition of metals from the burning of coal and human activity. An earlier peak in metal exposure suggests that selection on metal tolerance was likely much stronger 100 years ago, and metal exposure to modern populations of urban mammals is much less stressful relative to historical highs. Indeed, we found few negative effects of body metal content on measures of individual performance, including body length and relative cranial capacity. It is possible that our measures were too crude to capture more subtle variations in health at the time of specimen collection, but it is also likely that these negative results reflect the fact that metal levels are relatively lower today. It is less clear what these ecological patterns of metal exposure means for the evolution of tolerance to heavy metals—is there current relaxed selection on heavy metal tolerance? Could metal tolerance have facilitated adaptation to other pollutants? An exciting area of future research is the evolutionary implications of these ecological patterns. Finally, this work highlighted the potential ecological importance of manganese, a metal that has been studied for its neurotoxic effects in medical settings, but less so in ecological contexts.

Supplementary Information

Below is the link to the electronic supplementary material.Supplementary file1 (DOCX 210 KB)

Acknowledgements

We are grateful to the broader intellectual support and input of the Minneapolis-St Paul Urban Long-term Ecological Research program throughout the development of this project, including Sarah Hobbie, Cara Santelli, and Nic Jelinski. Members of the Snell-Rood lab provided valuable input on earlier versions of the manuscript. We are grateful to Naomi Wick for measuring the specimens in the original published morphological dataset used in the present analyses and to Becky Sponenburg at the QBIC Northwestern facility for running the ICP-MS measurements.

Author contribution

All authors contributed to the conception and design of the study. Savannah Kjaer performed all tissue sampling in the mammal collection with direction from curator Sharon Jansa. All spatial data was collected by Mary Marek-Spartz; all analyses run by Emilie Snell-Rood. The first draft of the manuscript was written by Emilie Snell-Rood with assistance in the discussion from Charlotte Devitz. All authors provided comments and edits on multiple drafts of the manuscript. All authors read and approved the final manuscript.

Funding

This research was supported by funding from the National Science Foundation to the Minneapolis-St Paul Urban Long-term Ecological Research Program (DEB-2045382) and the Minnesota Environment and Natural Resources Trust Fund as recommended by the Legislative-Citizen Commission on Minnesota Resources (LCCMR; ML2022 CH 94 ART SEC 2 SUB 08E APPR 2022).

Data availability

All data are archived with the MSP Long-term Ecological Research program through the Environmental Data Initiative: https://doi.org/10.6073/pasta/a880c4c755afc532bcee8b9ea66845ee

Declarations

Ethical approval

This research made use of natural history collections (Bell Museum of Natural History) and did not require additional permits or approvals.

Consent to participate

Not applicable—this research did not involve human subjects.

Consent for publication

Not applicable—this research did not involve human subjects.

Competing interests

The authors declare no competing interests.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
==== Refs
References

Agosta SJ Morton D Diet of the big brown bat, <i>Eptesicus fuscus</i>, from Pennsylvania and western Maryland Northeast Nat 2003 10 89 104 10.1656/1092-6194(2003)010[0089:DOTBBB]2.0.CO;2
Agosta SJ, Morton D (2003) Diet of the big brown bat, <i>Eptesicus fuscus</i>, from Pennsylvania and western Maryland. Northeast Nat 10:89–10410.1656/1092-6194(2003)010[0089:DOTBBB]2.0.CO;2
Ali H, Khan E, Ilahi I (2019) Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chem 2019:1–14. 10.1155/2019/6730305
Asami R, Matsumori T, Shinjo R, Uemura R, Miyaoka Y, Mizuyama M, Ise Y, Sakamaki T (2021) Reconstruction of ocean environment time series since the late nineteenth century using sclerosponge geochemistry in the northwestern subtropical Pacific. Prog Earth Planet Sci 8(1):38. 10.1186/s40645-021-00434-7
Babcock H Some observations on the food habits of the short-tailed shrew (Blarina brevicauda) Science 1914 40 526 530 10.1126/science.40.1032.526 17830253
Babcock H (1914) Some observations on the food habits of the short-tailed shrew (Blarina brevicauda). Science 40:526–53017830253 10.1126/science.40.1032.526
Baeten J A century of red water: mine waste, legacy contamination, and institutional amnesia in Minnesota’s Mesabi Iron Range Water History 2018 10 245 266 10.1007/s12685-018-0220-y
Baeten J (2018) A century of red water: mine waste, legacy contamination, and institutional amnesia in Minnesota’s Mesabi Iron Range. Water History 10:245–26610.1007/s12685-018-0220-y
Baker RTM Handy RD Davies SJ Snook JC Chronic dietary exposure to copper affects growth, tissue lipid peroxidation, and metal composition of the grey mullet, Chelon labrosus Mar Environ Res 1998 45 357 365 10.1016/S0141-1136(98)00098-1
Baker RTM, Handy RD, Davies SJ, Snook JC (1998) Chronic dietary exposure to copper affects growth, tissue lipid peroxidation, and metal composition of the grey mullet, Chelon labrosus. Mar Environ Res 45:357–36510.1016/S0141-1136(98)00098-1
Bakulski KM Seo YA Hickman RC Brandt D Vadari HS Hu H Park SK Heavy metals exposure and Alzheimer’s disease and related dementias J Alzheimers Dis 2020 76 1215 1242 10.3233/JAD-200282 32651318
Bakulski KM, Seo YA, Hickman RC, Brandt D, Vadari HS, Hu H, Park SK (2020) Heavy metals exposure and Alzheimer’s disease and related dementias. J Alzheimers Dis 76:1215–124232651318 10.3233/JAD-200282
Balachandran RC Mukhopadhyay S McBride D Veevers J Harrison FE Aschner M Haynes EN Bowman AB Brain manganese and the balance between essential roles and neurotoxicity J Biol Chem 2020 295 6312 6329 10.1074/jbc.REV119.009453 32188696
Balachandran RC, Mukhopadhyay S, McBride D, Veevers J, Harrison FE, Aschner M, Haynes EN, Bowman AB (2020) Brain manganese and the balance between essential roles and neurotoxicity. J Biol Chem 295:6312–632932188696 10.1074/jbc.REV119.009453
Bazzicalupo AL Ruytinx J Ke YH Coninx L Colpaert JV Nguyen NH Vilgalys R Branco S Fungal heavy metal adaptation through single nucleotide polymorphisms and copy-number variation Mol Ecol 2020 29 4157 4169 10.1111/mec.15618 32866320
Bazzicalupo AL, Ruytinx J, Ke YH, Coninx L, Colpaert JV, Nguyen NH, Vilgalys R, Branco S (2020) Fungal heavy metal adaptation through single nucleotide polymorphisms and copy-number variation. Mol Ecol 29:4157–416932866320 10.1111/mec.15618
Berglund Å Nyholm NEI Slow improvements of metal exposure, health- and breeding conditions of pied flycatchers (<i>Ficedula hypoleuca</i>) after decreased industrial heavy metal emissions Sci Total Environ 2011 409 4326 4334 10.1016/j.scitotenv.2011.07.004 21788063
Berglund Å, Nyholm NEI (2011) Slow improvements of metal exposure, health- and breeding conditions of pied flycatchers (<i>Ficedula hypoleuca</i>) after decreased industrial heavy metal emissions. Sci Total Environ 409:4326–433421788063 10.1016/j.scitotenv.2011.07.004
Bindler R Renberg I Klaminder J Bridging the gap between ancient metal pollution and contemporary biogeochemistry J Paleolimnol 2008 40 755 770 10.1007/s10933-008-9208-4
Bindler R, Renberg I, Klaminder J (2008) Bridging the gap between ancient metal pollution and contemporary biogeochemistry. J Paleolimnol 40:755–77010.1007/s10933-008-9208-4
Boquete MT Lang I Weidinger M Richards CL Alonso C Patterns and mechanisms of heavy metal accumulation and tolerance in two terrestrial moss species with contrasting habitat specialization Environ Exp Bot 2021 182 104336 10.1016/j.envexpbot.2020.104336
Boquete MT, Lang I, Weidinger M, Richards CL, Alonso C (2021) Patterns and mechanisms of heavy metal accumulation and tolerance in two terrestrial moss species with contrasting habitat specialization. Environ Exp Bot 182:104336. 10.1016/j.envexpbot.2020.10433610.1016/j.envexpbot.2020.104336
Buford KN Snidow CR Curiel TG Dark HE Purcell JB Grey DK Mrug S Knight DC Hippocampal and amygdala volumes vary with residential proximity to toxicants at Birmingham, Alabama’s 35th Avenue Superfund Site Behav Neurosci 2023 137 5 330 338 10.1037/bne0000564 37471045
Buford KN, Snidow CR, Curiel TG, Dark HE, Purcell JB, Grey DK, Mrug S, Knight DC (2023) Hippocampal and amygdala volumes vary with residential proximity to toxicants at Birmingham, Alabama’s 35th Avenue Superfund Site. Behav Neurosci 137(5):330–338. 10.1037/bne000056437471045 10.1037/bne0000564
Cardwell RD Deforest DK Brix KV Adams WJ Do Cd, Nu, Ni, Pb, and Zn biomagnifiy in acquatic ecosystems? Rev Environ Contam Toxicol 2013 226 101 122 23625131
Cardwell RD, Deforest DK, Brix KV, Adams WJ (2013) Do Cd, Nu, Ni, Pb, and Zn biomagnifiy in acquatic ecosystems? Rev Environ Contam Toxicol 226:101–12223625131
Cecil KM Pediatric exposures to neurotoxicants: a review of magnetic resonance imaging and spectroscopy findings Diagnostics 2022 12 3 641 10.3390/diagnostics12030641 35328193
Cecil KM (2022) Pediatric exposures to neurotoxicants: a review of magnetic resonance imaging and spectroscopy findings. Diagnostics 12(3):641. 10.3390/diagnostics1203064135328193 10.3390/diagnostics12030641
Cecil KM, Brubaker CJ, Adler CM, Dietrich KN, Altaye M, Egelhoff JC, Wessel S, Elangovan I, Hornung R, Jarvis K, Lanphear BP (2008) Decreased brain volume in adults with childhood lead exposure. PLoS Med 5(5):e112
Chadwick EA Simpson VR Nicholls AEL Slater FM Lead levels in Eurasian otters decline with time and reveal interactions between sources, prevailing weather, and stream chemistry Environ Sci Technol 2011 45 1911 1916 10.1021/es1034602 21294545
Chadwick EA, Simpson VR, Nicholls AEL, Slater FM (2011) Lead levels in Eurasian otters decline with time and reveal interactions between sources, prevailing weather, and stream chemistry. Environ Sci Technol 45:1911–191621294545 10.1021/es1034602
Datko-Williams L Wilkie A Richmond-Bryant J Analysis of U.S. soil lead (Pb) studies from 1970 to 2012 Sci Total Environ 2014 468 854 863 10.1016/j.scitotenv.2013.08.089 24076506
Datko-Williams L, Wilkie A, Richmond-Bryant J (2014) Analysis of U.S. soil lead (Pb) studies from 1970 to 2012. Sci Total Environ 468:854–86324076506 10.1016/j.scitotenv.2013.08.089
Dauwe T Bervoets L Pinxten R Blust R Eens M Variation of heavy metals within and among feathers of birds of prey: effects of molt and external contamination Environ Pollut 2003 124 429 436 10.1016/S0269-7491(03)00044-7 12758023
Dauwe T, Bervoets L, Pinxten R, Blust R, Eens M (2003) Variation of heavy metals within and among feathers of birds of prey: effects of molt and external contamination. Environ Pollut 124:429–43612758023 10.1016/S0269-7491(03)00044-7
Dobson AW Erikson KM Aschner M Manganese neurotoxicity Redox-Active Met Neurol Disord 2004 1012 115 128
Dobson AW, Erikson KM, Aschner M (2004) Manganese neurotoxicity. Redox-Active Met Neurol Disord 1012:115–128
Dubay SG Fuldner CC Bird specimens track 135 years of atmospheric black carbon and environmental policy Proc Natl Acad Sci USA 2017 114 11321 11326 10.1073/pnas.1710239114 29073051
Dubay SG, Fuldner CC (2017) Bird specimens track 135 years of atmospheric black carbon and environmental policy. Proc Natl Acad Sci USA 114:11321–1132629073051 10.1073/pnas.1710239114
Egendorf SP Mielke HW Castorena-Gonzalez JA Powell ET Gonzales CR Soil lead (Pb) in New Orleans: a spatiotemporal and racial analysis Int J Environ Res Public Health 2021 18 3 1314 10.3390/ijerph18031314 33535687
Egendorf SP, Mielke HW, Castorena-Gonzalez JA, Powell ET, Gonzales CR (2021) Soil lead (Pb) in New Orleans: a spatiotemporal and racial analysis. Int J Environ Res Public Health 18(3):1314. 10.3390/ijerph1803131433535687 10.3390/ijerph18031314
Eisler R (1988) Lead hazards to fish, wildlife and invertebrates: a synoptic review. U.S. Fish and Wildlife Service. Biol Rep 85(1.14). Contaminant Hazard Review Report No 14. https://semspub.epa.gov/work/03/137426.pdf
Ellis JL, Ponette-González AG, Fry M, Johnson JA (2023) Reduced reflectance and altered color: the potential cost of external particulate matter accumulation on urban Rock Pigeon (Columba livia) feathers. Front Ecol Evol 11:1-8. 10.3389/fevo.2023.946624
Elton S Bishop LC Wood B Comparative context of Plio-Pleistocene hominin brain evolution J Hum Evol 2001 41 1 27 10.1006/jhev.2001.0475 11414771
Elton S, Bishop LC, Wood B (2001) Comparative context of Plio-Pleistocene hominin brain evolution. J Hum Evol 41:1–2711414771 10.1006/jhev.2001.0475
Fang T Yang K Lu WX Cui K Li J Liang YY Hou GJ Zhao XX Li H An overview of heavy metal pollution in Chaohu Lake, China: enrichment, distribution, speciation, and associated risk under natural and anthropogenic changes Environ Sci Pollut Res 2019 26 29585 29596 10.1007/s11356-019-06210-x
Fang T, Yang K, Lu WX, Cui K, Li J, Liang YY, Hou GJ, Zhao XX, Li H (2019) An overview of heavy metal pollution in Chaohu Lake, China: enrichment, distribution, speciation, and associated risk under natural and anthropogenic changes. Environ Sci Pollut Res 26:29585–2959610.1007/s11356-019-06210-x
Farag AM Boese CJ Woodward DF Bergman HL Physiological-changes and tissue metal accumulation in rainbow-trout exposed to foodborne and waterborne metals Environ Toxicol Chem 1994 13 2021 2029 10.1002/etc.5620131215
Farag AM, Boese CJ, Woodward DF, Bergman HL (1994) Physiological-changes and tissue metal accumulation in rainbow-trout exposed to foodborne and waterborne metals. Environ Toxicol Chem 13:2021–202910.1002/etc.5620131215
Farmer JG Eades LJ Mackenzie AB Kirika A BaileyWatts TE Stable lead isotope record of lead pollution in Loch Lomond sediments since 1630 AD Environ Sci Technol 1996 30 3080 3083 10.1021/es960162o
Farmer JG, Eades LJ, Mackenzie AB, Kirika A, BaileyWatts TE (1996) Stable lead isotope record of lead pollution in Loch Lomond sediments since 1630 AD. Environ Sci Technol 30:3080–308310.1021/es960162o
Finarelli JA Estimation of endocranial volume through the use of external skull measures in the Carnivora (mammalia) J Mammal 2006 87 1027 1036 10.1644/05-MAMM-A-430R1.1
Finarelli JA (2006) Estimation of endocranial volume through the use of external skull measures in the Carnivora (mammalia). J Mammal 87:1027–103610.1644/05-MAMM-A-430R1.1
Finarelli JA Estimating endocranial volume from the outside of the skull in Artiodactyla J Mammal 2011 92 200 212 10.1644/09-MAMM-A-391.1
Finarelli JA (2011) Estimating endocranial volume from the outside of the skull in Artiodactyla. J Mammal 92:200–21210.1644/09-MAMM-A-391.1
Found C Helwig K The reliability of spot tests for the detection of arsenic and mercury in natural history collections: a case study Collection 1992 11 6 15
Found C, Helwig K (1992) The reliability of spot tests for the detection of arsenic and mercury in natural history collections: a case study. Collection 11:6–15
Gabrielli P Wegner A Sierra-Hernández MR Beaudon E Davis M Barker JD Thompson LG Early atmospheric contamination on the top of the Himalayas since the onset of the European Industrial Revolution Proc Natl Acad Sci USA 2020 117 3967 3973 10.1073/pnas.1910485117 32041888
Gabrielli P, Wegner A, Sierra-Hernández MR, Beaudon E, Davis M, Barker JD, Thompson LG (2020) Early atmospheric contamination on the top of the Himalayas since the onset of the European Industrial Revolution. Proc Natl Acad Sci USA 117:3967–397332041888 10.1073/pnas.1910485117
Galiciolli MEA Lima LS Costa NDD Andrade DPD Irioda AC Oliveira CS IQ alteration induced by lead in developed and underdeveloped/ developing countries: a systematic review and a meta-analysis Environ Pollut 2022 292 118316 10.1016/j.envpol.2021.118316 34648837
Galiciolli MEA, Lima LS, Costa NDD, Andrade DPD, Irioda AC, Oliveira CS (2022) IQ alteration induced by lead in developed and underdeveloped/ developing countries: a systematic review and a meta-analysis. Environ Pollut 292:118316. 10.1016/j.envpol.2021.11831634648837 10.1016/j.envpol.2021.118316
Gillikin DP Dehairs F Baeyens W Navez J Lorrain A André L Inter- and intra-annual variations of Pb/Ca ratios in clam shells (<i>Mercenaria mercenaria</i>): a record of anthropogenic lead pollution? Mar Pollut Bull 2005 50 1530 1540 10.1016/j.marpolbul.2005.06.020 16085111
Gillikin DP, Dehairs F, Baeyens W, Navez J, Lorrain A, André L (2005) Inter- and intra-annual variations of Pb/Ca ratios in clam shells (<i>Mercenaria mercenaria</i>): a record of anthropogenic lead pollution? Mar Pollut Bull 50:1530–154016085111 10.1016/j.marpolbul.2005.06.020
Goldsmith CD Scanlon PF Lead levels in small mammals and selected invertebrates associated with highways of different traffic densities Bull Environ Contam Toxicol 1977 17 311 316 10.1007/BF01686084 66960
Goldsmith CD, Scanlon PF (1977) Lead levels in small mammals and selected invertebrates associated with highways of different traffic densities. Bull Environ Contam Toxicol 17:311–31666960 10.1007/BF01686084
Green AJ Planchart A The neurological toxicity of heavy metals: a fish perspective Comp Biochem Physiol C: Toxicol Pharmacol 2018 208 12 19 29199130
Green AJ, Planchart A (2018) The neurological toxicity of heavy metals: a fish perspective. Comp Biochem Physiol C: Toxicol Pharmacol 208:12–1929199130
Gullson BL Gillings BR Lead exchange in teeth and bone–a pilot study using stable lead isotopes Environ Health Perspect 1997 105 820 824 9347897
Gullson BL, Gillings BR (1997) Lead exchange in teeth and bone–a pilot study using stable lead isotopes. Environ Health Perspect 105:820–8249347897
Han ZX Guo XY Zhang BM Liao JG Nie LS Blood lead levels of children in urban and suburban areas in China (1997–2015): Temporal and spatial variations and influencing factors Sci Total Environ 2018 625 1659 1666 10.1016/j.scitotenv.2017.12.315 29996461
Han ZX, Guo XY, Zhang BM, Liao JG, Nie LS (2018) Blood lead levels of children in urban and suburban areas in China (1997–2015): Temporal and spatial variations and influencing factors. Sci Total Environ 625:1659–166629996461 10.1016/j.scitotenv.2017.12.315
Hawks CA Williams SL Arsenic in natural history collections Leather Conserv News 1986 2 1 4
Hawks CA, Williams SL (1986) Arsenic in natural history collections. Leather Conserv News 2:1–4
Helander B Sundbom M Runkel AA Bignert A Temporal changes in concentrations of lead and other trace metals in free-ranging eurasian eagle owls <i>Bubo bubo</i> in Sweden Arch Environ Contam Toxicol 2019 77 377 389 10.1007/s00244-019-00654-5 31312864
Helander B, Sundbom M, Runkel AA, Bignert A (2019) Temporal changes in concentrations of lead and other trace metals in free-ranging eurasian eagle owls <i>Bubo bubo</i> in Sweden. Arch Environ Contam Toxicol 77:377–38931312864 10.1007/s00244-019-00654-5
Hollis L Hogstrand C Wood CM Tissue-specific cadmium accumulation, metallothionein induction, and tissue zinc and copper levels during chronic sublethal cadmium exposure in juvenile rainbow trout Arch Environ Contam Toxicol 2001 41 468 474 10.1007/s002440010273 11598784
Hollis L, Hogstrand C, Wood CM (2001) Tissue-specific cadmium accumulation, metallothionein induction, and tissue zinc and copper levels during chronic sublethal cadmium exposure in juvenile rainbow trout. Arch Environ Contam Toxicol 41:468–47411598784 10.1007/s002440010273
Honda K Min BY Tatsukawa R Distribution of heavy-metals and their age-related-changes in the Eastern great white egret, EGRETTA-ALBA-MODESTA, IN KOREA Arch Environ Contam Toxicol 1986 15 185 197 10.1007/BF01059967 3707203
Honda K, Min BY, Tatsukawa R (1986) Distribution of heavy-metals and their age-related-changes in the Eastern great white egret, EGRETTA-ALBA-MODESTA, IN KOREA. Arch Environ Contam Toxicol 15:185–1973707203 10.1007/BF01059967
Hoostal MJ Bidart-Bouzat MG Bouzat JL Local adaptation of microbial communities to heavy metal stress in polluted sediments of Lake Erie FEMS Microbiol Ecol 2008 65 156 168 10.1111/j.1574-6941.2008.00522.x 18559016
Hoostal MJ, Bidart-Bouzat MG, Bouzat JL (2008) Local adaptation of microbial communities to heavy metal stress in polluted sediments of Lake Erie. FEMS Microbiol Ecol 65:156–16818559016 10.1111/j.1574-6941.2008.00522.x
Hyvärinen H Tyni P Nieminen P Effects of moult, age, and sex on the accumulation of heavy metals in the otter (<i>Lutra lutra</i>) in Finland Bull Environ Contam Toxicol 2003 70 278 284 10.1007/s00128-002-0188-1 12545359
Hyvärinen H, Tyni P, Nieminen P (2003) Effects of moult, age, and sex on the accumulation of heavy metals in the otter (<i>Lutra lutra</i>) in Finland. Bull Environ Contam Toxicol 70:278–28412545359 10.1007/s00128-002-0188-1
Jacobson Y Incorporation of trace elements in aragonite skeletons of South East Mediterranean vermetids Appl Geochem 2023 155 105720 10.1016/j.apgeochem.2023.105720
Jacobson Y (2023) Incorporation of trace elements in aragonite skeletons of South East Mediterranean vermetids. Appl Geochem 155:105720. 10.1016/j.apgeochem.2023.10572010.1016/j.apgeochem.2023.105720
Janssens TKS Roelofs D van Straalen NM Molecular mechanisms of heavy metal tolerance and evolution in invertebrates Insect Sci 2009 16 3 18 10.1111/j.1744-7917.2009.00249.x
Janssens TKS, Roelofs D, van Straalen NM (2009) Molecular mechanisms of heavy metal tolerance and evolution in invertebrates. Insect Sci 16:3–1810.1111/j.1744-7917.2009.00249.x
Jones KC Symon C Taylor PJL Walsh J Johnston AE Evidence for a decline in rural herbage lead levels in the UK Atmos Environ Part a-Gen Top 1991 25 361 369 10.1016/0960-1686(91)90307-S
Jones KC, Symon C, Taylor PJL, Walsh J, Johnston AE (1991) Evidence for a decline in rural herbage lead levels in the UK. Atmos Environ Part a-Gen Top 25:361–36910.1016/0960-1686(91)90307-S
Kålås JA Steinnes E Lierhagen S Lead exposure of small herbivorous vertebrates from atmospheric pollution Environ Pollut 2000 107 21 29 10.1016/S0269-7491(99)00155-4 15093005
Kålås JA, Steinnes E, Lierhagen S (2000) Lead exposure of small herbivorous vertebrates from atmospheric pollution. Environ Pollut 107:21–2915093005 10.1016/S0269-7491(99)00155-4
Karri V Schuhmacher M Kumar V Heavy metals (Pb, Cd, As and MeHg) as risk factors for cognitive dysfunction: a general review of metal mixture mechanism in brain Environ Toxicol Pharmacol 2016 48 203 213 10.1016/j.etap.2016.09.016 27816841
Karri V, Schuhmacher M, Kumar V (2016) Heavy metals (Pb, Cd, As and MeHg) as risk factors for cognitive dysfunction: a general review of metal mixture mechanism in brain. Environ Toxicol Pharmacol 48:203–21327816841 10.1016/j.etap.2016.09.016
Kaushal SS Wood KL Galella JG Gion AM Haq S Goodling PJ Haviland KA Reimer JE Morel CJ Wessel B Making ‘chemical cocktails’–evolution of urban geochemical processes across the Periodic Table of elements Appl Geochem 2020 119 104632 10.1016/j.apgeochem.2020.104632
Kaushal SS, Wood KL, Galella JG, Gion AM, Haq S, Goodling PJ, Haviland KA, Reimer JE, Morel CJ, Wessel B (2020) Making ‘chemical cocktails’–evolution of urban geochemical processes across the Periodic Table of elements. Appl Geochem 119:104632. 10.1016/j.apgeochem.2020.10463210.1016/j.apgeochem.2020.104632
Klerks PL Weis JS Genetic adaptation to heavy-metals in aquatic organisms - a review Environ Pollut 1987 45 173 205 10.1016/0269-7491(87)90057-1 15092750
Klerks PL, Weis JS (1987) Genetic adaptation to heavy-metals in aquatic organisms - a review. Environ Pollut 45:173–20515092750 10.1016/0269-7491(87)90057-1
Lacerda D Pestana IA Vergilio CD de Rezende CE Global decrease in blood lead concentrations due to the removal of leaded gasoline Chemosphere 2023 324 138207 10.1016/j.chemosphere.2023.138207 36822521
Lacerda D, Pestana IA, Vergilio CD, de Rezende CE (2023) Global decrease in blood lead concentrations due to the removal of leaded gasoline. Chemosphere 324:138207. 10.1016/j.chemosphere.2023.13820736822521 10.1016/j.chemosphere.2023.138207
Lind Y Bignert A Odsjö T Decreasing lead levels in Swedish biota revealed by 36 years (1969–2004) of environmental monitoring J Environ Monit 2006 8 824 834 10.1039/B517867C 16896466
Lind Y, Bignert A, Odsjö T (2006) Decreasing lead levels in Swedish biota revealed by 36 years (1969–2004) of environmental monitoring. J Environ Monit 8:824–83416896466 10.1039/B517867C
Mason LH, Harp JP, Han DY (2014) Pb neurotoxicity: neuropsychological effects of lead toxicity. Biomed Res Int 2014:1–8. 10.1155/2014/840547
McConnell JR Edwards R Coal burning leaves toxic heavy metal legacy in the Arctic Proc Natl Acad Sci USA 2008 105 12140 12144 10.1073/pnas.0803564105 18711138
McConnell JR, Edwards R (2008) Coal burning leaves toxic heavy metal legacy in the Arctic. Proc Natl Acad Sci USA 105:12140–1214418711138 10.1073/pnas.0803564105
McConnell JR Wilson AI Stohl A Arienzo MM Chellman NJ Eckhardt S Thompson EM Pollard AM Steffensen JP Lead pollution recorded in Greenland ice indicates European emissions tracked plagues, wars, and imperial expansion during antiquity Proc Natl Acad Sci USA 2018 115 5726 5731 10.1073/pnas.1721818115 29760088
McConnell JR, Wilson AI, Stohl A, Arienzo MM, Chellman NJ, Eckhardt S, Thompson EM, Pollard AM, Steffensen JP (2018) Lead pollution recorded in Greenland ice indicates European emissions tracked plagues, wars, and imperial expansion during antiquity. Proc Natl Acad Sci USA 115:5726–573129760088 10.1073/pnas.1721818115
McConnell JR Chellman NJ Wilson AI Stohl A Arienzo MM Eckhardt S Fritzsche D Kipfstuhl S Opel T Place PF Steffensen JP Pervasive Arctic lead pollution suggests substantial growth in medieval silver production modulated by plague, climate, and conflict Proc Natl Acad Sci USA 2019 116 14910 14915 10.1073/pnas.1904515116 31285330
McConnell JR, Chellman NJ, Wilson AI, Stohl A, Arienzo MM, Eckhardt S, Fritzsche D, Kipfstuhl S, Opel T, Place PF, Steffensen JP (2019) Pervasive Arctic lead pollution suggests substantial growth in medieval silver production modulated by plague, climate, and conflict. Proc Natl Acad Sci USA 116:14910–1491531285330 10.1073/pnas.1904515116
McConnell JR, Maselli OJ, Sigl M, Vallelonga P, Neumann T, Anschütz H, Bales RC, Curran MAJ, Das SB, Edwards R, Kipfstuhl S, Layman L, Thomas ER (2014) Antarctic-wide array of high-resolution ice core records reveals pervasive lead pollution began in 1889 and persists today. Scientific Reports 4(1). 10.1038/srep05848
Meerts P Van Isacker N Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe Plant Ecol 1997 133 221 231 10.1023/A:1009717619579
Meerts P, Van Isacker N (1997) Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe. Plant Ecol 133:221–23110.1023/A:1009717619579
Mukhtar H Chan CY Lin YP Lin CM Assessing the association and predictability of heavy metals in avian organs, feathers, and bones using crowdsourced samples Chemosphere 2020 252 126583 10.1016/j.chemosphere.2020.126583 32443269
Mukhtar H, Chan CY, Lin YP, Lin CM (2020) Assessing the association and predictability of heavy metals in avian organs, feathers, and bones using crowdsourced samples. Chemosphere 252:126583. 10.1016/j.chemosphere.2020.12658332443269 10.1016/j.chemosphere.2020.126583
Nardiello V Fidalgo LE López-Beceiro A Bertero A Martínez-Morcillo S Míguez MP Soler F Caloni F Pérez-López M Metal content in the liver, kidney, and feathers of Northern gannets, Morus bassanus, sampled on the Spanish coast Environ Sci Pollut Res 2019 26 19646 19654 10.1007/s11356-019-05356-y
Nardiello V, Fidalgo LE, López-Beceiro A, Bertero A, Martínez-Morcillo S, Míguez MP, Soler F, Caloni F, Pérez-López M (2019) Metal content in the liver, kidney, and feathers of Northern gannets, Morus bassanus, sampled on the Spanish coast. Environ Sci Pollut Res 26:19646–1965410.1007/s11356-019-05356-y
Nava-Diaz R Hoogesteijn AL Erosa MD Febles JL Mendez-Gonzalez RM Comparative study of lead concentration in feathers of urban and rural passerines in Merida, Mexico Bull Environ Contam Toxicol 2015 95 470 474 10.1007/s00128-015-1628-z 26253842
Nava-Diaz R, Hoogesteijn AL, Erosa MD, Febles JL, Mendez-Gonzalez RM (2015) Comparative study of lead concentration in feathers of urban and rural passerines in Merida, Mexico. Bull Environ Contam Toxicol 95:470–47426253842 10.1007/s00128-015-1628-z
Nixon CM Worley DM McClain MW Food habits of squirrels in southeast Ohio J Wildl Manag 1968 32 2 294 305 10.2307/3798974
Nixon CM, Worley DM, McClain MW (1968) Food habits of squirrels in southeast Ohio. J Wildl Manag 32(2):294–305. 10.2307/379897410.2307/3798974
Nyholm N Rühling Å Effects of decreased atmospheric heavy metal deposition in South Sweden on terrestrial birds and small mammals in natural populations Water Air Soil Pollut Focus 2001 1 439 448 10.1023/A:1017582305685
Nyholm N, Rühling Å (2001) Effects of decreased atmospheric heavy metal deposition in South Sweden on terrestrial birds and small mammals in natural populations. Water Air Soil Pollut Focus 1:439–44810.1023/A:1017582305685
O’Neal SL Zheng W Manganese toxicity upon overexposure: a decade in review Curr Environ Health Rep 2015 2 315 328 10.1007/s40572-015-0056-x 26231508
O’Neal SL, Zheng W (2015) Manganese toxicity upon overexposure: a decade in review. Curr Environ Health Rep 2:315–32826231508 10.1007/s40572-015-0056-x
Oflaherty EJ Physiologically based models for bone-seeking elements: V. Lead Absorption and Disposition in Childhood Toxicol Appl Pharmacol 1995 131 297 308 10.1006/taap.1995.1072 7716770
Oflaherty EJ (1995) Physiologically based models for bone-seeking elements: V. Lead Absorption and Disposition in Childhood. Toxicol Appl Pharmacol 131:297–3087716770 10.1006/taap.1995.1072
Papadopulos AST Helmstetter AJ Osborne OG Comeault AA Wood DP Straw EA Mason L Fay MF Parker J Dunning LT Foote AD Smith RJ Lighten J Rapid parallel adaptation to anthropogenic heavy metal pollution Mol Biol Evol 2021 38 3724 3736 10.1093/molbev/msab141 33950261
Papadopulos AST, Helmstetter AJ, Osborne OG, Comeault AA, Wood DP, Straw EA, Mason L, Fay MF, Parker J, Dunning LT, Foote AD, Smith RJ, Lighten J (2021) Rapid parallel adaptation to anthropogenic heavy metal pollution. Mol Biol Evol 38:3724–373633950261 10.1093/molbev/msab141
Pfalzer AC Bowman AB Relationships between essential manganese biology and manganese toxicity in neurological disease Curr Environ Health Rep 2017 4 223 228 10.1007/s40572-017-0136-1 28417441
Pfalzer AC, Bowman AB (2017) Relationships between essential manganese biology and manganese toxicity in neurological disease. Curr Environ Health Rep 4:223–22828417441 10.1007/s40572-017-0136-1
Polak-Juszczak L Trace elements in the livers of cod (<i>Gadus morhua L.</i>) from the Baltic Sea: levels and temporal trends Environ Monit Assess 2013 185 687 694 10.1007/s10661-012-2584-2 22371038
Polak-Juszczak L (2013) Trace elements in the livers of cod (<i>Gadus morhua L.</i>) from the Baltic Sea: levels and temporal trends. Environ Monit Assess 185:687–69422371038 10.1007/s10661-012-2584-2
Qian N, Boyle EA, Zhou LP, Tanzil J, Chen QQ, Zhang S, Chen ML (2023) Spatial-temporal variability and sources of lead (Pb) in the Indian Ocean and Asian Marginal Seas. J Geophys Res Oceans 128(2):e2022JC019222. 10.1029/2022JC019222
Robards K Worsfold P Cadmium - toxicology and analysis - a review Analyst 1991 116 549 568 10.1039/an9911600549 1928728
Robards K, Worsfold P (1991) Cadmium - toxicology and analysis - a review. Analyst 116:549–5681928728 10.1039/an9911600549
Rubio-Franchini I Rico-Martínez R Evidence of lead biomagnification in invertebrate predators from laboratory and field eperiments Environ Pollut 2011 159 1831 1835 10.1016/j.envpol.2011.03.021 21530032
Rubio-Franchini I, Rico-Martínez R (2011) Evidence of lead biomagnification in invertebrate predators from laboratory and field eperiments. Environ Pollut 159:1831–183521530032 10.1016/j.envpol.2011.03.021
Sakai ST Arsznov BM Lundrigan BL Holekamp KE Virtual endocasts: an application of computed tomography in the study of brain variation among hyenas Ann N Y Acad Sci 2011 1225 E160 E170 10.1111/j.1749-6632.2011.05988.x 21599694
Sakai ST, Arsznov BM, Lundrigan BL, Holekamp KE (2011) Virtual endocasts: an application of computed tomography in the study of brain variation among hyenas. Ann N Y Acad Sci 1225:E160–E17021599694 10.1111/j.1749-6632.2011.05988.x
Scheuhammer AM Effects of acidification on the availability of toxic metals and calcium to wild birds and mammals Environ Pollut 1991 71 329 375 10.1016/0269-7491(91)90036-V 15092123
Scheuhammer AM (1991) Effects of acidification on the availability of toxic metals and calcium to wild birds and mammals. Environ Pollut 71:329–37515092123 10.1016/0269-7491(91)90036-V
Seo JS Lee SH Won HS Yang M Nahm SS Nam SM Effects of gestational and lactational lead exposure and high fat diet feeding on cerebellar development of postnatal rat offspring Nutrients 2023 15 20 4325 10.3390/nu15204325 37892401
Seo JS, Lee SH, Won HS, Yang M, Nahm SS, Nam SM (2023) Effects of gestational and lactational lead exposure and high fat diet feeding on cerebellar development of postnatal rat offspring. Nutrients 15(20):4325. 10.3390/nu1520432537892401 10.3390/nu15204325
Shen GT Boyle EA Lead in corals - reconstruction of historical industrial fluxes to the surface ocean Earth Planet Sci Lett 1987 82 289 304 10.1016/0012-821X(87)90203-2
Shen GT, Boyle EA (1987) Lead in corals - reconstruction of historical industrial fluxes to the surface ocean. Earth Planet Sci Lett 82:289–30410.1016/0012-821X(87)90203-2
Shull AF Habits of the short-tailed shrew, Blarina brevicauda (Say) Am Nat 1907 41 495 522 10.1086/278820
Shull AF (1907) Habits of the short-tailed shrew, Blarina brevicauda (Say). Am Nat 41:495–52210.1086/278820
Shultz AJ Adams BJ Bell KC Ludt WB Pauly GB Vendetti JE Natural history collections are critical resources for contemporary and future studies of urban evolution Evol Appl 2021 14 233 247 10.1111/eva.13045 33519967
Shultz AJ, Adams BJ, Bell KC, Ludt WB, Pauly GB, Vendetti JE (2021) Natural history collections are critical resources for contemporary and future studies of urban evolution. Evol Appl 14:233–24733519967 10.1111/eva.13045
Snell-Rood EC Wick N Anthropogenic environments exert variable selection on cranial capacity in mammals Proc R Soc B-Biol Sci 2013 280 1769 20131384 10.1098/rspb.2013.1384
Snell-Rood EC, Wick N (2013) Anthropogenic environments exert variable selection on cranial capacity in mammals. Proc R Soc B-Biol Sci 280(1769):20131384. 10.1098/rspb.2013.138410.1098/rspb.2013.1384
Snell-Rood E, Kjaer S, Marek-Spartz M, Devitz C, Jansa S (2024) Heavy metals in mammal tissue over the last 100 years and their proximity to populated places in Minnesota ver 1. Environ Data Initiative. Accessed 2024-07-24. 10.6073/pasta/a880c4c755afc532bcee8b9ea66845ee
Swier VJ (2003) Food habits of big brown bats (Eptesicus fuscus) in Sioux Falls, South Dakota, Proceedings of the South Dakota Academy of Science. South Dakota Academy of Sciences, 82:73
Talmage SS Walton BT Food chain transfer and potential renal toxicity of mercury to small mammals at a contaminated terrestrial field site Ecotoxicology 1993 2 243 256 10.1007/BF00368533 24201735
Talmage SS, Walton BT (1993) Food chain transfer and potential renal toxicity of mercury to small mammals at a contaminated terrestrial field site. Ecotoxicology 2:243–25624201735 10.1007/BF00368533
Tuschl K Mills PB Clayton PT Manganese and the brain Int Rev Neurobiol 2013 110 277 312 10.1016/B978-0-12-410502-7.00013-2 24209443
Tuschl K, Mills PB, Clayton PT (2013) Manganese and the brain. Int Rev Neurobiol 110:277–31224209443 10.1016/B978-0-12-410502-7.00013-2
van Straalen NM van Wensem J Heavy metal content of forest litter arthropods as related to body-size and trophic level Environ Pollut Series A, Ecol Biol 1986 42 209 221 10.1016/0143-1471(86)90032-2
van Straalen NM, van Wensem J (1986) Heavy metal content of forest litter arthropods as related to body-size and trophic level. Environ Pollut Series A, Ecol Biol 42:209–22110.1016/0143-1471(86)90032-2
Whitaker JO Jr Food of Mus musculus, Peromyscus maniculatus bairdi and Peromyscus leucopus in Vigo County, Indiana J Mammal 1966 47 473 486 10.2307/1377688
Whitaker JO Jr (1966) Food of Mus musculus, Peromyscus maniculatus bairdi and Peromyscus leucopus in Vigo County, Indiana. J Mammal 47:473–48610.2307/1377688
Wiener JG Sandheinrich MB Contaminants in the Upper Mississippi River: historic trends, responses to regulatory controls, and emerging concerns Hydrobiologia 2010 640 49 70 10.1007/s10750-009-0064-7
Wiener JG, Sandheinrich MB (2010) Contaminants in the Upper Mississippi River: historic trends, responses to regulatory controls, and emerging concerns. Hydrobiologia 640:49–7010.1007/s10750-009-0064-7
Witmer LM Ridgely RC Dufeau DL Semones MC Endo H Frey R Using CT to peer into the past: 3D visualization of the brain and ear regions of birds, crocodiles, and nonavian dinosaurs Anatomical imaging: towards a new morphology 2008 Tokyo Springer Japan 67 87
Witmer LM, Ridgely RC, Dufeau DL, Semones MC (2008) Using CT to peer into the past: 3D visualization of the brain and ear regions of birds, crocodiles, and nonavian dinosaurs. In: Endo H, Frey R (eds) Anatomical imaging: towards a new morphology. Springer Japan, Tokyo, pp 67–87
Wolff JO The effects of density, food, and interspecific interference on home range size in Peromyscus leucopus and Peromyscus maniculatus Can J Zool 1985 63 2657 2662 10.1139/z85-397
Wolff JO (1985) The effects of density, food, and interspecific interference on home range size in Peromyscus leucopus and Peromyscus maniculatus. Can J Zool 63:2657–266210.1139/z85-397
Xin Z Wenchao Z Zhenguang Y Yiguo H Zhengtao L Xianliang Y Xiaonan W Tingting L Liming Z Species sensitivity analysis of heavy metals to freshwater organisms Ecotoxicology 2015 24 1621 1631 10.1007/s10646-015-1500-2 26104218
Xin Z, Wenchao Z, Zhenguang Y, Yiguo H, Zhengtao L, Xianliang Y, Xiaonan W, Tingting L, Liming Z (2015) Species sensitivity analysis of heavy metals to freshwater organisms. Ecotoxicology 24:1621–163126104218 10.1007/s10646-015-1500-2
Yokel RA Blood-brain barrier flux of aluminum, manganese, iron and other metals suspected to contribute to metal-induced neurodegeneration J Alzheimers Dis 2006 10 223 253 10.3233/JAD-2006-102-309 17119290
Yokel RA (2006) Blood-brain barrier flux of aluminum, manganese, iron and other metals suspected to contribute to metal-induced neurodegeneration. J Alzheimers Dis 10:223–25317119290 10.3233/JAD-2006-102-309
