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Article

Homing Pigeons as Biomonitors of Atmospheric Metal Exposure and Health Effects to Promote Environment Sustainability

by
Jia Cui
1,2,
Richard S. Halbrook
3,
Shuying Zang
1,4,*,
Mary A. Masdo
5,
Li Sun
1 and
Shuang Han
6
1
Heilongjiang Province Key Laboratory of Geographical Environment Monitoring and Spatial Information Service in Cold Regions, Harbin Normal University, Harbin 150025, China
2
School of Economics and Management, Harbin Normal University, Harbin 150025, China
3
Cooperative Wildlife Research Laboratory and Department of Zoology (Emeritus), Southern Illinois University, Carbondale, IL 62901, USA
4
Heilongjiang Province Collaborative Innovation Center of Cold Region Ecological Safety, Harbin 150025, China
5
TG&G Wildlife Consulting, Carbondale, IL 62902, USA
6
Institute for Environmental and Climate Research, Jinan University, Guangzhou 511443, China
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(16), 7014; https://doi.org/10.3390/su16167014
Submission received: 27 July 2024 / Revised: 9 August 2024 / Accepted: 12 August 2024 / Published: 15 August 2024
(This article belongs to the Special Issue Impact of Heavy Metals on the Sustainable Environment)
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Abstract

:
Homing pigeons are promising biomonitors of atmospheric metal pollution that may influence human health and environmental sustainability. However, exact interactions between respiratory and oral exposure and associations between atmospheric and pulmonary metal concentrations and effects are lacking. The current experiments measure differences in homing pigeon tissue cadmium, lead, and mercury concentrations due to diet and atmospheric exposure, and changes in pulmonary lesions associated with changing seasonal atmospheric metal concentrations. Forty 6-week-old homing pigeons were raised for 9 months in experiment 1, and seventy-five pigeons from different age groups were necropsied in winter, spring/summer, and autumn in experiment 2. Results indicate that atmospheric metal concentrations influence lung cadmium and lead concentrations, that atmospheric metal concentrations fluctuated seasonally and were greatest in fine particulate matter (PM2.1) during winter, and the rate of lung cadmium and lead accumulations reflected temporal changes. There were significant correlations between lung metal concentrations and alveolar macrophage lesions. Time (10 months) and higher metal concentrations (266 ng/g for Cd and 16,442 ng/g for Pb) are both important factors in the production of pulmonary dust cells. Our experiments indicate that homing pigeons can provide specific information on diseases resulting from atmospheric pollution exposure and that these data can assist in public health decisions and environmental regulations to promote sustainable development of the environment.

1. Introduction

Atmospheric pollution in urban areas is a major worldwide concern with potential adverse impacts on terrestrial species and environment sustainability [1,2,3,4]. Many atmospheric pollutants (e.g., heavy metals, polyaromatic hydrocarbons, polychlorinated biphenyls, etc.) are bound to airborne fine particles that are readily inhaled by humans and wildlife [5], potentially causing or exacerbating respiratory diseases [6,7,8]. Mechanical air monitoring is commonly used to provide data on atmospheric concentrations of various pollutants; however, the use of animal species as biomonitors provides additional data not available from mechanical air monitoring systems. Wild species integrate multiple atmospheric contaminants over temporal and spatial scales, thus providing bioavailability, bioaccumulation, and effects data that enhance the understanding of exposure [9,10,11].
Avian species are potentially valuable biomonitors and have previously been used to evaluate environmental pollutants [12,13,14]. Specifically, feral pigeons (Columba livia) are a cosmopolitan avian species that has been recommended for environmental monitoring [15,16]. However, semi-tame homing pigeons, which are feral pigeons that have been bred for site fidelity and are raised by racing pigeon hobbyists in many countries [17,18], provide location, diet, and age data not available with feral pigeons. Homing Pigeon Associations in many countries (i.e., the United States, China, Philippines, Belgium, etc.) are supported by many members in numerous urban and rural areas that can potentially supply known aged pigeons to support research activities.
Because homing pigeons are relatively long-lived (18+ years), spend their life at the same location, are exposed to the same atmosphere as humans, and the age, diet, and life histories are known, they provide useful data for evaluating potential adverse atmospheric effects on human health [19]. Histological evaluation of homing pigeon lung tissue also provides specific information on diseases resulting from atmospheric contaminant exposure that may assist in public health decisions and the development of environmental sustainability. For example, previous studies have linked exposure to atmospheric Cd with human lung cancer, and exposure to atmospheric heavy metals during gestation and the first few weeks of life with pediatric asthma [6,7]. Contaminant concentrations measured in homing pigeon lung tissue would provide epidemiolocal evidence of exposure and accumulation, thus supporting medical practitioners in the diagnosis and treatment of human lung diseases, as well as providing public health officials with data useful in developing regulations needed to reduce atmospheric contaminant concentrations and exposure.
The atmosphere is continually changing and therefore contaminants in the atmosphere are also in a state of flux [20]. Like humans, homing pigeons are continuously breathing the surrounding air, and thus are exposed to whatever contaminants are in the air during each inhalation, whether the contaminants are present only periodically (perhaps resulting from an accidental release, pesticide spraying, or some irregular pulsing) or present on a more, or less, continuous basis (daily factory releases, traffic exhaust, coal burning, etc.) [19,20,21,22,23]. Results of previous studies indicate that environmental contaminants, including polyaromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), mercury (Hg), cadmium (Cd), and lead (Pb), accumulate in the lung, liver, kidney, and/or feathers of homing pigeons collected from China [19,24,25], Philippines (unpublished), and the United States. Therefore, we know that monitored contaminants were bioavailable and accumulating in monitored homing pigeons, but we are uncertain of the exact interactions between respiratory and oral routes of exposure. Although some homing pigeon studies have suggested that inhaled organic pollutants are the main exposure route for body burdens [19], although exposure to metals is less certain. Our current experiments attempt to address this question by comparing contaminant concentrations in pigeon food and between homing pigeons with varying respiratory exposure.
Regardless of the route of exposure, our previous studies provide evidence that exposure is chronic rather than acute [24], whether from ingestion or respiratory routes. Our previous research also has reported that Pb and Cd concentrations in lung tissue of same-aged homing pigeons collected from Beijing and Guangzhou, China, closely reflected atmospheric concentrations of those metals in the two cities. However, lung tissue responses to atmospheric contaminants exposure are complex and involve innate and adaptive defenses [26]. In humans, adverse respiratory health effects (pneumonia, asthma, chronic obstructive pulmonary disease) have resulted from exposure to inhaled particulate matter [27,28]. Atmospheric particulate matter is a carrier of various toxic and harmful pollutants. Heavy metals in fine particulate matter are a serious environmental and health concern in China, particularly during winter. Harbin is located at high latitude with long and cold winters, which is not conducive to gas diffusion and requires long-term heating. Complex terrain and meteorological conditions also impede the dispersion of pollutants in Beijing. Motor vehicle and coal combustion emissions are major contributors to elemental pollutants on PM2.5 in Beijing and Harbin [29,30]. Studies have reported alveolar macrophages (dust cells) and airway epithelial cells are responsible for initiating local responses (inflammation) in lung tissue following inhalation of particulate matter [26]. We have observed gray/black lesions in the distal lung margins of homing pigeons collected from Beijing, China [24], and Manila, Philippines (unpublished), which may indicate phagocytosis of inhaled carbon particulate matter. These lesions suggest that the clearance mechanisms in the studied pigeons may be overwhelmed by excessive particulate exposure, potentially resulting in diminished respiratory capacity; however, our previous studies did not quantify effects associated with observed gray/black lung margins. The current study provides histological data demonstrating an association between atmospheric particulate metal concentrations and alveolar macrophages.
There also are questions regarding temporal changes in contaminant concentrations in air and whether measured concentrations in pigeon lung tissue would reflect those changes. If atmospheric pollution in an urban area is improving or worsening, would the contaminant concentrations in pigeon lung tissue mirror those changes? The current study, in part, addresses this question by mechanically measuring seasonal changes in atmospheric metal concentrations and comparing those changes with metal concentrations in lung tissue of homing pigeons collected during similar time periods. We hypothesize that metal concentrations measured in homing pigeon lung tissue will mirror metal concentrations measured in atmospheric particulate matter. Our specific objectives are as follows: (1) to clarify differences in accumulation of measured metal contaminant concentrations in homing pigeon tissues due to ingestion and respiratory routes of exposure; (2) to compare seasonal accumulated Cd, Pb, and Hg concentrations in homing pigeon lung tissue with seasonal changes in atmospheric concentrations measured using passive mechanical air monitors; (3) to evaluate correlations between Cd, Pb, and Hg concentrations measured in homing pigeon lung tissues and observed lung histological lesions; and (4) to develop a protocol for use of homing pigeons as a biomonitor of atmospheric contaminants to promote environment sustainability in urban areas.

2. Materials and Methods

2.1. Experimental Design and Tissue Collection

2.1.1. Experiment 1

On 1 November 2015, 40 6-week-old homing pigeons were obtained from cooperating homing pigeon hobbyist in Beijing (n = 20) and Harbin (n = 20), China (Figure 1 and Figure S1). Pigeons from Beijing were collected from a loft located approximately 1 km from Peking University and pigeons from Harbin were collected from the Nangang District of Harbin city center. For 9 months (1 November 2015 through 31 July 2016), 10 randomly selected 6-week-old pigeons from each location were caged within the loft in which they were hatched (caged pigeons), the remaining 10 6-week-old pigeons from each location were allowed to fly freely (free-flying), which is the normal homing pigeon practice. At each location, the same food source was provided to caged and free-flying pigeons according to normal pigeon husbandry protocols. At the end of the 9-month experimental period, pigeons were killed by cervical dislocation and necropsied. Breast feathers were collected and stored in paper envelopes at room temperature prior to Cd, Pb, and Hg analyses. Lungs were removed and a slice of lung tissue was stored in 10% formaldehyde prior to histological analysis, and the remaining lung tissue along with liver and kidney tissues was wrapped in aluminum foil and stored at −20 °C prior to metal analyses.
On the day the 20 6-week-old pigeons were selected at each location, and on the first day of each month thereafter, 5 g of food provided to the monitored pigeons at each location was collected and stored at room temperature prior to metal analyses. At the same time, monthly air monitoring data were obtained from a mechanical air sampler placed near the pigeon collection location in Harbin.

2.1.2. Experiment 2

Ten 4-month-old, and five 1-, 5-, and 10-year-old pigeons, each (25 total), were collected at the beginning of April, August, and December 2018 from the same pigeon loft in Harbin where pigeons were collected during experiment 1 (Figure 1). Four-month-old pigeons necropsied on 1 April represent those exposed to the Harbin atmosphere from December through March (winter), those necropsied on August 1 represent those exposed from April through July (spring/summer), and those necropsied on December 1 represent pigeons exposed from August through November (autumn). Pigeons were killed by cervical dislocation and necropsied on the day of collection. During necropsy, lungs were removed, and a small slice of each lung was placed in 10% formaldehyde prior to histological preparations, and the remaining lung tissue was wrapped in aluminum foil and stored at −20 °C prior to metal analyses.

2.2. Lung Tissue Histology

Collected lung histology samples were placed in 10% formaldehyde for 48 h, dried in a series of ethanol baths, cleared with xylene, and embedded in paraffin wax. Five-micrometer-thick tissue sections were cut using a microtome and stained with hematoxylin and eosin (H&E) prior to microscopic evaluation. Three sections of each tissue were double-blind evaluated by two researchers under a high-power optical microscope and the severity of alveolar macrophages (Dust cells) and inflammatory cell infiltration scored between 1 and 6. Scoring of 1, 2, 3, 4, 5, and 6 corresponded to <1, 5, 10, 15, 20, and 30+%, respectively, of the histological sample involving the pathological lesion.

2.3. Particulate Matters Collection and Processing

A Tisch Model No. TE-20-800 air sampler (Tisch Environmental Inc., Cleves, OH, USA) was placed next to the pigeon loft where pigeons were collected in Harbin during experiments 1 and 2. Particulate matter was collected for 30-day periods during both experiments 1 and 2 using Tisch Quartz Microfiber Filters (TE-20-301-QZ and TE-20-305-QZ, Tisch Environmental Inc., Cleves, OH, USA). Eight different particulate matter diameters (0.4 μm, 0.7 μm, 1.1 μm, 2.1 μm, 3.3 μm, 4.7 μm, 5.8 μm, 9 μm, 10 μm) were collected using low volume air flow (28.3 L/min). Detailed information on the Tisch Ambient Eight-Stage Cascade Impactor is described in Text S1. Sampling procedures followed US EPA National Ambient Air Quality Standard [31].
Prior to use, quartz microfiber filters were heated at 450 °C for 4 h to remove organic matter and then cooled in a desiccator for 24 h prior to use. After sampling, the filters were put in a desiccator for 24 h and then into a clean filter box and stored at 4 °C prior to metal analyses.
For analysis, 1/4 of each filter was cut into fragments using Teflon scissor and then dissolved in a mixture of 6 mL HNO3 (Merck, Darmstadt, Germany), 2 mL HCL, and 2 mL HF (Sinopharm Chemical Reagent Co., Ltd., Shanghai, China). After 1 h, the samples were placed in a microwave oven (Mars-5, CEM Company, Matthews, NC, USA) and the temperature was raised to 130 °C within 8 min and maintained for 10 min, raised to 150 °C within 8 min and maintained for 10 min, and finally, the temperature was raised to 185 °C within 8 min and maintained for 10 min. Samples were removed from the microwave and cooled to room temperature. Afterward, 1 mL of HCLO4 was added to the samples and placed on an acid-driven processor below 110 °C. Once the volume of material in the crucible reached approximately 1–2 mL, heating was stopped. Each digested sample was transferred to a 50 mL polypropylene test tube, the digestion vessel was rinsed three times with Milli-Q deionized water (Millipore, Bedford, MA, USA), and the digested sample was diluted to a final volume of 50 mL with ultra-pure water.

2.4. Contaminant Analyses and Quality Control

Cadmium, Pb, and Hg concentrations in pigeon food, pigeon tissues, and atmospheric samples were measured by inductively coupled plasma mass spectrometry (ICP-MS, Agilent 7500cx, Agilent Technologies Inc., Palo Alto, CA, USA) following USEPA Method 3050B and USEPA Method 200.8, respectively. Detailed methods and quality control have previously been described (Text S1) [24].

2.5. Data Analysis

Descriptive and inferential statistical analyses were performed using SPSS 20.0. Independent-sample t-test was used to evaluate differences between male and female pigeon tissues. Nonparametric statistical methods (e.g., Mann–Whitney U Test) were used to evaluate differences in tissue metal concentrations and histology lesions between caged and free-flying pigeons collected from Beijing and Harbin, and differences in metal concentrations in pigeon food between Beijing and Harbin. Nonparametric statistical methods (e.g., Kruskal–Wallis Test) were used to evaluate differences in metal concentrations in lung tissue during the three time periods in experiment 2, differences in contaminant concentrations and histology results among age groups, and among the three time periods of experiment 2. A Pearson correlation was used to evaluate the relationship between metal concentrations and histology lesions in the lung tissues of pigeons in experiments 1 and 2. A Dixon’s Q-test was used to evaluate outliers and a p value less than 0.05 was considered statistically significant. The concentrations of metals in the tissues are expressed as ng/g dry weight (dw).

3. Results

3.1. Metal Accumulation under Ingestion and Respiratory Routes of Exposure (Experiment 1)

3.1.1. Metal Accumulation Characteristics of Pigeon Tissues

There were no significant differences in metal concentrations evaluated in any tissues between male and female pigeons (Tables S1 and S2); therefore, metal concentrations in male and female pigeons were combined. Harbin caged and free-flying pigeons had significantly greater Cd concentrations in all tissues and Pb concentrations in feather and lung tissue of free-flying pigeons compared to similar pigeons from Beijing (Table S3 and Figure 2). Cadmium and Pb concentrations were consistently greater in tissues of free-flying pigeons compared to caged pigeons collected in Harbin, although the difference was only significant in lung Cd concentrations and feather Pb concentrations. Mercury concentrations measured in all evaluated tissues of free-flying and caged pigeons from Harbin were similar. Cadmium, Pb, and Hg concentrations were similar among all tissues evaluated in free-flying and caged pigeons from Beijing, except that liver Cd concentrations were significantly greater in caged compared to free-flying pigeons (Table S3 and Figure 2).

3.1.2. Metal Concentrations in Pigeon Food

Cadmium concentration measured in Harbin pigeon food ( x ¯ = 20.1 ng/g, n = 10) was significantly greater (p = 0.010) than concentrations measured in Beijing pigeon food ( x ¯ = 11.7 ng/g, n = 15). There were no significant differences in Hg and Pb concentrations measured in pigeon food collected from Beijing and Harbin (Table S4).

3.1.3. Metal Concentrations in Atmospheric Particulate Matter

The seasonal concentrations of evaluated metals on different-size atmospheric particulate matter followed a similar pattern (Figure 3). Particulate matter concentrations of Cd, Hg, and Pb were much greater in winter (December through February) and lowest during summer (June and July). The greatest metal concentrations were distributed in PM0.7, PM1.1, and PM2.1 particulate sizes during each season monitored, while the least metal concentrations were measured on particulate sizes 0.4 and 4.7–10 (Figure 3). During the 9-month sampling period, mean concentrations of Cd and Hg were greatest on PM2.1 particulate size ( x ¯ = 266.96 ng/g for Cd, x ¯ = 24.35 ng/g for Hg, n = 9). During winter, concentrations of Pb on PM0.7, PM1.1, and PM2.1 were similar and much greater than concentrations measured on other particulate matter diameters ( x ¯ = 39,469.57 ng/g for PM2.1, x ¯ = 40244.50 ng/g for PM1.1, x ¯ = 39,386.23 ng/g for PM0.7, n = 9). The least metal concentrations were measured on PM0.4 fraction ( x ¯ = 10.24 ng/g for Cd, x ¯ = 2.95 ng/g for Hg, x ¯ = 1770.20 ng/g for Pb, n = 9).

3.2. Seasonal Metal Concentrations Measured in Atmospheric Particulate Matter and Homing Pigeon Lung Tissue (Experiment 2)

Cadmium, Hg, and Pb concentrations measured on PM2.1 particulate matter followed a similar seasonal pattern as observed during experiment 1 with the greatest metal concentrations occurring during the winter and the least metal concentrations occurring during summer (Figure 3 and Figure 4D). There were significant increases in lung Cd and Pb concentrations in 1-yo pigeons collected in Harbin from 1 December 2017 through 1 December 2018 (Figure 4A,C). There were no significant differences in lung Hg concentrations in 1-yo pigeons among the three time periods studied. Lung Hg concentrations in 5-yo Harbin pigeons increased significantly from winter to spring/summer but then decreased during autumn (Figure 4B). Lung Cd and Pb concentrations were not significantly different in 5-yo pigeons during the three seasons studied.
Lung Cd, Pb, and Hg concentrations in 10-yo pigeons were not significantly different among the three seasons studied; however, lung Cd concentrations in 10-yo pigeons were significantly greater than Cd concentrations in 4-month, 1-yo, and 5-yo pigeons during all time periods evaluated (Figure 4A). During winter and spring/summer periods, lung Pb concentrations significantly increased (p = 0.002) with pigeon age (Figure 4C). During autumn, lung Pb concentrations in 10-yo pigeons were greater than Pb concentrations in 4-month, 1-yo, and 5-yo pigeons, although the difference was not statistically significant (Figure 4C). During winter and autumn, lung Hg concentrations in 10-yo pigeons were significantly greater than Hg concentrations in young pigeons (Figure 4B). There were no significant differences in lung Hg concentrations among age groups in homing pigeons necropsied in August (Figure 4B).

3.3. Histology Analysis of Lung Tissue

3.3.1. Histology Analysis (Experiment 1)

The incidence of pneumoconiosis in lung tissue histological samples was significantly greater in both caged (p = 0.001) and free-flying (p < 0.001) pigeons raised in Harbin compared to those raised in Beijing (Figure 5A). All free-flying pigeons from Harbin (n = 9) had alveolar macrophage (dust cell) scores of 4 or 5, while 90% of the caged pigeons from Harbin (n = 11) had alveolar macrophage scores ≥ 4. In contrast, only two free-flying and one caged pigeon from Beijing had pneumoconiosis based on alveolar macrophage scores > 1.
There were significant positive correlations (p < 0.01) between Harbin and Beijing pigeon (n = 40) lung alveolar macrophage scores and lung Cd and Pb concentrations (Table S6, Figure 5D–F). There were no significant differences in inflammatory cell infiltration scores between caged and free-flying pigeons raised in Beijing or those raised in Harbin (Figure 5A).

3.3.2. Histology Analysis (Experiment 2)

Histological evaluations indicated serious inflammatory cell infiltration in 4-month-old pigeons necropsied on 1 August and 1 December 2018 (Figure 5B). The incidence of lung inflammatory cell infiltration was significantly greater (p = 0.022) in 4-month-old pigeons necropsied on 1 August and 1 December 2018, compared to those necropsied on 1 April 2018 (Figure 5B). Lung inflammatory cell infiltration scores were significantly greater (p = 0.020) in 4-month-old pigeons necropsied on 1 December 2018, compared to 1-, 5-, and 10-yo pigeons necropsied on that date; however, there were no significant differences in lung inflammatory cell infiltration scores among 1-, 5-, and 10-yo pigeons necropsied during any of the three time periods of experiment 2 (Figure 5B).
The incidence of lung alveolar macrophages (dust cells) significantly increased (p = 0.001) in 4-month-old pigeons necropsied on 1 April, 1 August, and 1 December 2018 (Figure 5C). Lung alveolar macrophage scores were significantly greater in 1-, 5-, and 10-yo pigeons compared to 4-month-old pigeons necropsied on 1 April (p = 0.033) and 1 August 2018 (p = 0.012); however, there were no differences in lung alveolar macrophage scores among different aged pigeons necropsied on 1 December 2018 (Figure 5C). Lung alveolar macrophage scores were significantly correlated with lung Cd, Pb, and Hg concentrations measured in pigeons necropsied during experiment 2 (Figure 5G–I, Table S6).

4. Discussion

4.1. Ingestion and Respiratory Routes of Exposure

Our first experiment was designed to evaluate differences in the accumulation of measured metal concentrations in homing pigeon tissues due to ingestion and respiratory routes of exposure. Our hypothesis was that increased respiratory exposure associated with flight (i.e., increased respiratory demand) would result in greater lung tissue metal concentrations in free-flying compared to caged pigeons. For pigeons evaluated in Harbin, Cd and Pb concentrations were greater in all tissues of free-flying pigeons compared to caged pigeons, thus providing evidence that atmospheric exposure contributed to body burdens and supporting our hypothesis. Significant increases in Cd in lung tissues of free-flying pigeons are most noteworthy and indicate that pigeon lung tissue can serve as a monitor of atmospheric metal exposure.
Although our data support the hypothesis that respiratory exposure does result in increased accumulation of metals in homing pigeon lung tissues, there are extenuating circumstances that potentially influence metal accumulation in avian tissues. Internal respiratory defensive mechanisms (inflammatory cell infiltration and alveolar macrophage activity) and sequestering and elimination of metals during feather mold, potentially influence metal concentrations in evaluated pigeon tissues. For example, Pb concentrations in feathers of free-flying pigeons from Harbin were 5.1, 3.7, and 1.6 times greater than concentrations in lung, liver, and kidney tissue, respectively. These data suggest that sequestering of Pb in pigeon feathers may significantly influence Pb concentrations in other tissues and therefore may complicate interpretation of results.
In addition, Cd concentrations were significantly greater in food fed to Harbin pigeons compared to food fed to Beijing pigeons, which may result from different manufacturer production and quality control in pigeon food purchased in Beijing and Harbin (Table S4), thus confounding direct comparison of Cd concentrations in pigeon tissues between the two cities. As would be expected, given increased Cd concentrations in Harbin food, lung, liver, and kidney Cd concentrations were significantly greater in Harbin pigeons compared to Beijing pigeons regardless of whether the pigeons were caged or free-flying (Table S3, Figure 2C,D). However, Hg and Pb concentrations were not significantly different in pigeon food collected from Harbin and Beijing and there were no significant differences in Hg and Pb concentrations in pigeon liver or kidney tissues between the two cities whether caged or free-flying (Tables S3 and S4). As expected, these results indicate that metal concentrations in the diet of homing pigeons potentially contribute to measured concentrations in liver and kidney tissues. These findings are contrary to previously reported studies evaluating organic pollutants (PAHs, PCBs) in homing pigeons [19]. In that study, atmospheric organic pollutant exposure, and not dietary exposure, was reported to be the source of liver concentrations in studied homing pigeons.
Even with these confounding factors, Cd concentrations in lung tissue of free-flying pigeons from Harbin were significantly greater than concentrations in lung tissue of caged pigeons from Harbin, and also greater than caged or free-flying pigeons from Beijing. In addition, Pb concentrations in lung tissue of free-flying pigeons from Harbin were significantly greater than lung concentrations in free-flying pigeons from Beijing. If lung Cd and Pb concentrations only resulted from diet, there should be no significant differences in lung Cd concentrations between caged and free-flying pigeons in Harbin or Pb concentrations between free-flying pigeons from Harbin and those from Beijing. These results suggest that lung tissue concentrations of Cd and Pb reflect, at least in part, concentrations of these metals in the Harbin atmosphere.
We did not detect a difference in lung Pb or Hg concentration between caged and free-flying pigeons from Harbin; however, Pb concentrations in feathers of free-flying pigeons were significantly greater than concentrations in feathers of caged pigeons (Table S3). While feather Hg concentrations were also greater in free-flying pigeons compared to caged pigeons, the difference was not statistically significant (Table S3). These results further support the conclusion that sequestering of metals in feathers, and subsequent removal during feather molt, can influence results regarding respiratory and/or ingestion exposure in avian species.
Although we detected differences in lung metal concentrations between caged and free-flying pigeons in Harbin, there were no significant increases in any metal concentrations in lung tissue between caged and free-flying pigeons collected from Beijing. Although we did not measure atmospheric metal concentrations in Beijing, results do not indicate that atmospheric metal concentrations influenced tissue metal concentrations in evaluated Beijing pigeons. In addition, histological data do not indicate significant atmospheric exposure-related pulmonary disease in Beijing pigeons as was observed in Harbin homing pigeons. During 2013, the government of China implemented an Air Pollution Prevention and Control Action Plan designed to significantly reduce atmospheric particulate pollution [32]. Our biomonitoring results, along with other atmospheric studies in Beijing, provide supporting evidence that the Action Plan has successfully improved air quality and promoted environmental sustainability in Beijing [33,34].

4.2. Tissue and Atmospheric Particulate Matter Metal Concentrations

Because of confounding factors that may influence tissue metal concentrations in 5- and 10-yo pigeons (i.e., length and potential fluctuations in exposure making it difficult to compare atmospheric metal concentrations with pigeon lung concentrations), here we will focus on metal concentrations and accumulation in 4-month-old and 1-yo pigeons, except to report that, as with our previous research [24], Cd concentrations in all tissues and Pb concentrations in lung tissues increased with age. During experiments 1 and 2, Cd, Pb, and Hg concentrations measured on PM2.1 size atmospheric particulate matter were greatest during winter, decreased during spring/summer, and increased again in autumn (Figure 4D), which is consistent with a previous study [35]. Although we have not identified the specific source of the atmospheric metals, the pattern follows that observed with the use of coal as a heating fuel in Harbin (Figure 4D). Previous studies in China also have reported that coal combustion associated with heating demands resulted in increased emissions of PM1.0 and PM2.5 and associated heavy metals [28,36]. Especially in Harbin, located in the far north of China, the main enriched elements originate from coal combustion used for heating during winter [37].
Lung Cd and Pb concentrations in 1-yo pigeons increased 1.9 and 23.3 ng/g, respectively, between 1 April and 1 August 2018, and increased 8.6 and 52.6 ng/g, respectively, between 1 August and 1 December 2018 (Figure 4A). Although Cd and Pb concentrations measured on PM2.1 size atmospheric particles were greatest in winter, decreased in spring/summer, and increased again in autumn (Figure 4D), lung Cd and Pb concentrations continually increased throughout the year (Figure 4A,C), although the rate of increase fluctuated and reflected changes in atmospheric metal concentrations in small size atmospheric particulate matter.
Seasonal fluctuations in lung metal concentrations in free-flying pigeons < 1 yo reflected seasonal changes in atmospheric concentrations (Figure 6). In experiment 1, lung Cd, Pb, and Hg accumulation rates in Harbin free-flying pigeons were 1.51, 8.83, and 0.56 ng/g each month, respectively, while lung:PM2.1 ratios were 5.66% for Cd, 0.54% for Pb, and 23% for Hg. For 4-month-old pigeons in experiment 2, lung Cd and Pb monthly accumulation rates were greater in winter and autumn (1.79 ng/g), while lung Pb monthly accumulation rates were greater in autumn (18.25 ng/g), both were least in spring/summer (−0.13 for Cd and 2.75 for Pb), which is similar to seasonal changes in metal concentrations of atmospheric PM2.1 (Figure 6). Similarly, during experiment 2, lung:PM2.1 ratios for 4-month-old pigeons were greatest for Cd in winter (5.99%) and Pb in autumn (0.97%) and least in spring/summer (−0.42% for Cd and 0.34% for Pb) (Figure 6). These data further support our conclusion that homing pigeon lung tissue metal concentrations are associated with metal concentrations in atmospheric particulate matter.
There are several biological/behavioral factors that may influence the concentrations of metals in homing pigeon tissues that need to be considered in interpreting these results. As previously discussed, the decreased rate of accumulation of some metals in avian tissues during August and September may be associated with sequestering and elimination of metals in feathers during the autumn molting [38,39]. In addition, the increased flying of younger pigeons during training sessions in spring, in preparation for summer racing, increases respiratory exposure that may result in increased lung metal exposure and accumulation. These biological/behavioral factors, along with knowledge that metal concentrations in the diet of homing pigeons from different locations may vary, are important considerations in the interpretation of research results. Regardless of these potentially confounding factors, our biomonitoring data support a conclusion that seasonal fluctuations in atmospheric metal concentrations are reflected in homing pigeon lung tissue, thus supporting our hypothesis that metal concentrations measured in homing pigeon lung tissue mirror metal concentrations measured on atmospheric particulate matter.

4.3. Evaluation of the Toxic Effects of Atmospheric Pollution on Homing Pigeon

Many epidemiological studies have investigated the effects of atmospheric heavy metal exposure on pulmonary function and disease [6,7,40,41]. Because of ethical considerations, it is difficult to directly measure contaminants in human lung tissue or to identify specific lesions of exposure and effects. Other researchers have relied on in vitro studies using cell cultures, or biomarkers in human tissues, i.e., DNA adducts in human blood to evaluate lung lesions associated with atmospheric contaminant exposure. Researchers also have used feral pigeons to assess contaminant exposure and potential adverse effects [16]. As far as we are aware, our studies [24], and research recently reported by Pei et al., 2017 and Tong et al., 2022, are the only studies that have used homing pigeons as a biomonitor [19,25]. Although studies previously referenced have indicated an association between environmental contaminants and exposure, studies using homing pigeons as a biomonitor report direct evidence of atmospheric contaminants in lung tissue and associated lung lesions. In the current study, we have demonstrated that metal concentrations measured in homing pigeon lung tissue are reflective of metal concentrations measured on atmospheric particulate matter in Harbin, China. Our results also indicated that lung Cd and Pb concentrations in free-flying homing pigeons from Harbin were significantly greater than concentrations in free-flying pigeons collected from Beijing, and the incidence of lesions in lungs of Harbin pigeons (dust cells) were significantly greater [i.e., 100% with serious (scores ≥ 4) dust cells] compared to lung lesions detected in Beijing pigeons (i.e., 20% with dust cell scores > 1).
In addition to dust cells, 20% of Harbin pigeons presented with severe cases of inflammatory cell infiltration (i.e., scores ≥ 4). Pigeons necropsied during experiment 1 were ~10 months old and the incidence of inflammatory cell infiltration observed in their lungs (mean score = 1.6) was not drastically different from 1-yo pigeons necropsied during experiment 2 (mean score = 2.5) (Figure 5A,B). Similarly, alveolar macrophage scores in lungs of pigeons necropsied during experiment 1 (mean score = 3.9) were similar to alveolar macrophage scores (mean score = 3.7) observed in lungs of 1-yo pigeons necropsied during experiment 2 (Figure 4A,C). In addition, the greater incidence of dust cells in the lungs of older pigeons collected from Harbin suggests that lung disease increases with age. Time and higher metal concentrations may be both important factors in the production of pulmonary dust cells (Figure 6). These data, along with correlations between metal concentrations and the incidence of dust cells, suggest that the incidence of lung disease is prevalent in the studied pigeons from Harbin and suggests that similar diseases may occur in other wild species or humans exposed to the same atmosphere. These results indicate the value of homing pigeons as biomonitors of atmospheric contaminant exposure and effects, which can assist in environmental regulations and environmental sustainability.

5. Conclusions

Atmospheric pollutants are predominantly bound to airborne fine particles that are readily inhaled by humans and animals and have adverse impacts on health and environmental sustainability. This study clarifies differences in accumulation due to oral and respiratory routes of exposure, indicates that metals measured in homing pigeon lung tissue reflect atmospheric metal concentrations, and that metal accumulation rates in lung tissues changed with metal concatenations in atmospheric PM2.1. Trace metal concentrations followed a similar trend with the greatest concentrations measured during winter on PM2.1, PM1.1, and PM0.7 fractions. Lung cadmium and lead accumulation rates of young free-flying pigeons were 1.51 and 8.83 ng/g each month and lung/PM2.1 ratios were 5.66% for Cd and 0.54% for Pb. Because of the increased probability of inhalation of smaller diameter particle sizes into lung bronchial and alveolar spaces, there is an increased likelihood for accumulation and adverse effects resulting from inhalation of metals attached to these particulate sizes. Increased concentrations of Cd measured on PM2.1, PM1.1, and PM0.7 particle sizes in Harbin atmosphere, increased Cd concentrations measured in lungs of free-flying pigeons compared to caged pigeons from Harbin, and a correlation between lung Cd concentrations and observed histological lesions support this assertion. Time (10 months) and higher metal concentrations (266 ng/g for Cd and 16,442 ng/g for Pb) are both important factors in the production of pulmonary dust cells. Our experiments add to existing data indicating that homing pigeons can provide specific information on diseases resulting from atmospheric pollution exposure and that these data may assist in the evaluation of public health and environmental regulations to promote environmentally sustainable development. Our research adds to existing knowledge that homing pigeons can serve as valuable biomonitors of atmospheric exposure and effects.
Although we provide sufficient data for the development of a protocol for using homing pigeons as a biomonitor in urban environments, there are some limitations. In our current study, atmospheric metals were a concern while other contaminants (e.g., polyaromatic hydrocarbons) are potentially also present in particulate matter. Our future plans are to measure a suite of organic and inorganic contaminants on atmospheric particulate matter and in lung tissue of exposed homing pigeons. We have evaluated associations between atmospheric metals and homing pigeon pulmonary metal concentrations and effects and future studies should also evaluate associations between lesions observed in homing pigeons and those reported in humans exposed to the same atmosphere, especially children.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su16167014/s1, Text S1: Materials and Methods; Table S1: Detailed information of individual homing pigeons collected from Harbin and Beijing, China during experiment 1; Table S2: Statistical differences in tissue metal concentrations between male and female homing pigeons collected during experiment 1; Table S3: Mean concentration (±SEM, ng/g) of heavy metals in feather, lung, kidney, and liver tissues of homing pigeon collected from Beijing and Harbin, China, during November 2015–July 2016 in experiment 1; Table S4: Metal concentrations (±SEM, ng/g) of metals measured in pigeon food collected from Beijing and Harbin, China, during experiment 1; Table S5: Detailed information of individual homing pigeons collected from Harbin, China, during experiment 2; Table S6: Pearson correlation between metal concentrations and histology scores in the lung tissues of homing pigeons in experiment 1 (n = 40) and experiment 2 (n = 75).

Author Contributions

Conceptualization, J.C., R.S.H. and S.Z.; formal analysis, J.C.; investigation, J.C., R.S.H., M.A.M., L.S. and S.H.; resources, S.Z.; data curation, J.C.; writing—original draft preparation, J.C.; writing—review and editing, R.S.H.; supervision, R.S.H. and S.Z.; project administration, S.Z.; funding acquisition, J.C. and S.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Key Joint Program of the National Natural Science Foundation of China (NSFC) and Heilongjiang Province for Regional Development (No. U20A2082), Natural Science Foundation of Heilongjiang Province of China (No. TD2019D002), Youth Project of the National Natural Science Foundation of China (No. 41701574), Excellent Youth Project of the Natural Science Foundation of Heilongjiang Province, China (No. YQ2021D009), and the Fundamental Research Funds for the Universities of Heilongjiang Province (No. 2022-KYYWF-0160).

Institutional Review Board Statement

The animal study protocol was approved by the Research Ethics Committee of Harbin Normal University (HNUARIA2023006).

Informed Consent Statement

Not applicable.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors on request.

Acknowledgments

The authors thank the pigeon hobbyist for this assistance and for providing the pigeons used in our research.

Conflicts of Interest

Author Mary A. Masdo was employed by the company TG&G Wildlife Consulting, Carbondale. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Figure 1. Sampling areas in Beijing and Harbin, China.
Figure 1. Sampling areas in Beijing and Harbin, China.
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Figure 2. Mean heavy metal concentration (±SEM, ng/g) measured in lung (A), feather (B), liver (C), and kidney (D) tissues of caged (c) and free-flying (f) 10-month-old homing pigeon collected from Beijing and Harbin, China, and necropsied 31 July 2016.
Figure 2. Mean heavy metal concentration (±SEM, ng/g) measured in lung (A), feather (B), liver (C), and kidney (D) tissues of caged (c) and free-flying (f) 10-month-old homing pigeon collected from Beijing and Harbin, China, and necropsied 31 July 2016.
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Figure 3. Seasonal mean metal concentrations (ng/g) measured on atmospheric particulate matter (A), and seasonal mean metal concentrations [Cd (B), Hg (C), Pb (D)] measured on different size atmospheric particulate matter during 1 November 2015 through 31 July 2016 in Harbin, China.
Figure 3. Seasonal mean metal concentrations (ng/g) measured on atmospheric particulate matter (A), and seasonal mean metal concentrations [Cd (B), Hg (C), Pb (D)] measured on different size atmospheric particulate matter during 1 November 2015 through 31 July 2016 in Harbin, China.
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Figure 4. Mean seasonal Cd (A), Hg (B), and Pb (C) concentrations (±SEM) measured in lung tissue of different aged homing pigeons (n = 75) collected from Harbin, China, on 1 April (Win.), 1 August (Spr./Sum.), and 1 December (Aut.) during 2018. Mean seasonal metal concentrations (D) measured on PM2.1 size atmospheric particulate matter collected monthly during 1 December–1 March (Win.), 1 April–1 August (Spr./Sum.), and 1 September–1 December (Aut.) in Harbin, China during 2017–2018. p value and * indicate significant differences among different periods and different age groups by Kruskal–Wallis Test.
Figure 4. Mean seasonal Cd (A), Hg (B), and Pb (C) concentrations (±SEM) measured in lung tissue of different aged homing pigeons (n = 75) collected from Harbin, China, on 1 April (Win.), 1 August (Spr./Sum.), and 1 December (Aut.) during 2018. Mean seasonal metal concentrations (D) measured on PM2.1 size atmospheric particulate matter collected monthly during 1 December–1 March (Win.), 1 April–1 August (Spr./Sum.), and 1 September–1 December (Aut.) in Harbin, China during 2017–2018. p value and * indicate significant differences among different periods and different age groups by Kruskal–Wallis Test.
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Figure 5. Mean (±SEM) inflammatory cell infiltration and dust cell histological lesion scores measured in lung tissue of 10-month-old homing pigeons collected 31 July 2016 from Harbin and Beijing, China (n = 20, each, c and f refers to pigeons that were caged or free-flying, respectively, * indicates significant difference between pigeons from Harbin and those from Beijing) (A). Mean (±SEM) inflammatory cell infiltration scores (B) and dust cell scores (C) measured in lung tissue collected from different aged homing pigeons from Harbin, China 1 April (Win.), 1 August (Spr./Sum.), and 1 December (Aut.) 2018 (* indicates significant differences among Win., Spr./Sum., and Aut. time periods and different age groups). Correlation between Cd (D), Hg (E), Pb (F) concentrations (ng/g) and dust cell histological scores measured in lung tissue of homing pigeons collected from Harbin and Beijing (n = 40) 31 July 2016. Correlation between Cd (G), Hg (H), Pb (I) concentrations and dust cell histological scores measured in lung tissue of homing pigeons (n = 75) collected from Harbin, China, during 2018 (* indicates significant correlation at 0.05 level, ** indicates significant correlation at 0.01 level). Histological lesions observed in lung tissue of homing pigeons collected from Harbin (J) and Beijing (K) during 2016, blue arrows point to inflammatory cell infiltration, and yellow arrows point to dust cells.
Figure 5. Mean (±SEM) inflammatory cell infiltration and dust cell histological lesion scores measured in lung tissue of 10-month-old homing pigeons collected 31 July 2016 from Harbin and Beijing, China (n = 20, each, c and f refers to pigeons that were caged or free-flying, respectively, * indicates significant difference between pigeons from Harbin and those from Beijing) (A). Mean (±SEM) inflammatory cell infiltration scores (B) and dust cell scores (C) measured in lung tissue collected from different aged homing pigeons from Harbin, China 1 April (Win.), 1 August (Spr./Sum.), and 1 December (Aut.) 2018 (* indicates significant differences among Win., Spr./Sum., and Aut. time periods and different age groups). Correlation between Cd (D), Hg (E), Pb (F) concentrations (ng/g) and dust cell histological scores measured in lung tissue of homing pigeons collected from Harbin and Beijing (n = 40) 31 July 2016. Correlation between Cd (G), Hg (H), Pb (I) concentrations and dust cell histological scores measured in lung tissue of homing pigeons (n = 75) collected from Harbin, China, during 2018 (* indicates significant correlation at 0.05 level, ** indicates significant correlation at 0.01 level). Histological lesions observed in lung tissue of homing pigeons collected from Harbin (J) and Beijing (K) during 2016, blue arrows point to inflammatory cell infiltration, and yellow arrows point to dust cells.
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Figure 6. Correlations between Cd, Pb, and Hg concentrations measured on atmospheric particulate matter (size PM2.1) and metal concentrations measured in lung tissue and dust cells of free-flying young (newborn and 4-month-old) homing pigeons collected from Harbin, China, during each time period of experiments 1 and 2. Column 1 = atmospheric metal concentrations, Column 2 = lung metal concentrations, Column 3 = lung/PM2.1 metal ratios, and Column 4 = representative pigeon lung histological photos.
Figure 6. Correlations between Cd, Pb, and Hg concentrations measured on atmospheric particulate matter (size PM2.1) and metal concentrations measured in lung tissue and dust cells of free-flying young (newborn and 4-month-old) homing pigeons collected from Harbin, China, during each time period of experiments 1 and 2. Column 1 = atmospheric metal concentrations, Column 2 = lung metal concentrations, Column 3 = lung/PM2.1 metal ratios, and Column 4 = representative pigeon lung histological photos.
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MDPI and ACS Style

Cui, J.; Halbrook, R.S.; Zang, S.; Masdo, M.A.; Sun, L.; Han, S. Homing Pigeons as Biomonitors of Atmospheric Metal Exposure and Health Effects to Promote Environment Sustainability. Sustainability 2024, 16, 7014. https://doi.org/10.3390/su16167014

AMA Style

Cui J, Halbrook RS, Zang S, Masdo MA, Sun L, Han S. Homing Pigeons as Biomonitors of Atmospheric Metal Exposure and Health Effects to Promote Environment Sustainability. Sustainability. 2024; 16(16):7014. https://doi.org/10.3390/su16167014

Chicago/Turabian Style

Cui, Jia, Richard S. Halbrook, Shuying Zang, Mary A. Masdo, Li Sun, and Shuang Han. 2024. "Homing Pigeons as Biomonitors of Atmospheric Metal Exposure and Health Effects to Promote Environment Sustainability" Sustainability 16, no. 16: 7014. https://doi.org/10.3390/su16167014

APA Style

Cui, J., Halbrook, R. S., Zang, S., Masdo, M. A., Sun, L., & Han, S. (2024). Homing Pigeons as Biomonitors of Atmospheric Metal Exposure and Health Effects to Promote Environment Sustainability. Sustainability, 16(16), 7014. https://doi.org/10.3390/su16167014

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