Dynamics of Heavy Metals in the Blood of House Sparrows (Passer domesticus) Across Different Urban Habitats in Meknes, Morocco

doi:10.21203/rs.3.rs-4707607/v1

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Dynamics of Heavy Metals in the Blood of House Sparrows (Passer domesticus) Across Different Urban Habitats in Meknes, Morocco

https://doi.org/10.21203/rs.3.rs-4707607/v1

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This study examines the accumulation of heavy metals (lead, cadmium, and zinc) in the blood of house sparrows (Passer domesticus) across various urban habitats in Meknes, Morocco. Fifty adult sparrows were captured from five distinct sites, including industrial, high-traffic, and rural areas. Blood samples were analyzed using Inductively Coupled Plasma Atomic Emission Spectroscopy (ICP-AES). Results show significant variations in heavy metal concentrations depending on the site. The highest levels were found in the industrial zone, with lead (Pb) at 336.02 µg/L, cadmium (Cd) at 12.28 µg/L, and zinc (Zn) at 1736.09 µg/L. Principal Component Analysis (PCA) and K-means clustering revealed three distinct pollution clusters: Cluster 0 (high Zn, low Pb and Cd), Cluster 1 (moderate levels of all metals), and Cluster 2 (high levels of all metals). These findings highlight the ecological and health risks associated with urban pollution and the value of house sparrows as effective bioindicators.

Heavy metals

bio indicators

urban pollution

house sparrows

ICP-AES

principal component analysis

Over the last century, the increase in industrial activities, traffic, and intensive agriculture has led to severe environmental pollution (Gomes da Silva & Gouveia, 2020). Heavy metals are considered critical contaminants in the environment due to their high potential to enter and accumulate in food chains (Yan et al., 2020; Kumar et al., 2019). Toxic metals such as lead (Pb) and cadmium (Cd) can have adverse effects on various physiological systems, including endocrine systems, at environmentally relevant concentrations (Balali-Mood et al., 2021). Some metals, at very specific doses, are essential for the life of organisms and are known as trace elements, necessary for biological processes, such as zinc (Wang, Li, & Zhou, 2020).

Numerous studies reporting variations in metal accumulation in urban birds have demonstrated a significant relationship between atmospheric metal concentration, traffic density, available food, and habitat sites (Kouddane et al., 2016; Haddadi et al., 2023; Richard et al., 2021).

Just like pigeons, house sparrows (Passer domesticus) feed on the ground and present abundant and stable populations, primarily associated with human activities (Silva-Ortega et al., 2023; Kouddane et al., 2016). Their environmental exposure in urban areas, similar to that of the human population, includes not only atmospheric exposure to pollutants such as heavy metals, but also to other sources of contamination like urban waste and contaminated runoff (Silva-Ortega et al., 2023). This diversity of exposures makes house sparrows (Passer domesticus) particularly useful bioindicators for monitoring pollution in urban environments, thus reflecting the overall impact of human activities on urban habitats (Swaileh & Sansur, 2006).

The present study examines the levels of lead, cadmium, and zinc in the blood of house sparrows, residing at varying distances from the city of Meknes. In urban areas, this species is sedentary, forming discrete flocks that remain faithful to specific feeding and resting areas (García-Arroyo et al., 2023). For this reason, a sample of birds is expected to reflect any variation in metal exposure at the local level.

Sample collection

The sample collection took place from December 2022 to mid-January 2023, with the approval of the High Commission for Water and Forests. Fifty adult house sparrows (Passer domesticus) were captured at various sites across the city of Meknes. These sites were selected to represent a range of urban areas and one rural area, in order to compare heavy metals bioaccumulation levels in the birds' Blood. Specific sites included the Industrial Zone (IZ), which has intense industrial activity; the Sidi Said Bus Station (SS), an urban area with medium traffic density; the Meknes Town Centre (TC), a high-density population and traffic area; the Fes Meknes Main Road (MR), a major roadway with heavy traffic; and a Rural Site (Ref), located close to the city, serving as a reference for zinc bioaccumulation comparisons.

The sparrows were captured using Japanese nets, an effective and humane method that minimizes stress and risk of injury (Clewley et al. 2018) Fig. 1.

Ethical Blood Collection and Anesthesia Protocol for House Sparrows

Blood samples from house sparrows were carefully collected from the right jugular vein, preferred for its width and ease of access. The bird was held firmly, the area was sterilized with alcohol, and a needle was inserted at a 15-degree angle. Blood was drawn gently, ensuring not to exceed 1% of the bird's body mass, in accordance with Owen's (2011) and Nimra et al.'s (2023) recommendations. The method cited by Kramer and Harris (2010) minimizes stress and pain for the bird, ensuring a safe collection without significant adverse effects on the bird's health or behavior.

To ensure ethical and humane practices in animal research, general anesthesia with isoflurane was performed in accordance with ethical standards for animal research, as detailed by Mehmannavaz et al. (2015) and Nakatsu et al. (2017), Rehman et al., (2020),the guidelines of the American Veterinary Medical Association (AVMA), and confirmed by the Ethics Committee of Moulay Ismail University in Meknes. Isoflurane was recommended for several reasons: rapid induction, easy maintenance of anesthesia, minimal impact on cardiopulmonary functions, and quick recovery, making it a preferred choice for anesthetizing house sparrows.

Isoflurane Anesthesia Protocol

Isoflurane is an inhaled anesthetic used to induce general anesthesia in animals, particularly favored for its rapid induction, quick recovery, and easy control of anesthetic depth in avian species specially small ones. Despite its potential myocardial depressant effects, it remains widely utilized in veterinary practice (Rehman et al., 2020).

For house sparrows, the necessary equipment included an induction chamber, an isoflurane bottle, an oxygen tank, sterile syringes and needles, gloves, and an anesthesia mask. Isoflurane was mixed with oxygen. The sparrow was placed in the induction chamber with an oxygen flow rate of 1–2 liters per minute and an isoflurane concentration of 3–5%, until it was anesthetized in 2 to 3 minutes. The absence of withdrawal reflexes and regular breathing were verified. Approximately 0.25 to 0.35 ml (250–350 µL) of blood was drawn, not exceeding 1% of the bird's body mass (Nimra et al. 2023). After blood collection, isoflurane administration was stopped for the bird's gradual recovery, and the bird was monitored until it resumed normal breathing.

Sample analysis

After centrifugation of the blood samples collected in EDTA tubes, 0.25–0.35 ml of plasma was treated with 1 ml of 65% nitric acid for a pre-digestion at room temperature for 24 hours. The samples were then subjected to mineralization in Teflon bombs at 120°C under pressure (20–40 bars) for 4 hours, using a microwave digestion system. After cooling, the clear solution obtained was diluted to a final volume with distilled water for the analysis of heavy metals. Microwave-assisted acid digestion is an effective and reliable method for the analysis of heavy metals in various sample matrices, (Mohamed et al., 2020; Papadopoulos et al., 2022). The concentrations of cadmium (Cd), lead (Pb), and zinc (Zn) in the blood samples of sparrows were quantified at the Research Center of the Faculty of Sciences at Moulay Ismail University in Meknes, using an ICPE-9000 ICP-AES spectrometer. The samples were exposed to high-energy plasma, and the characteristic light emissions of each metal were measured to determine their concentrations. The spectrometer was set up with a radio frequency power of 1.20 kW and gas flows adjusted for optimal analysis: 10.0 L/min for the plasma gas, 0.60 L/min for the auxiliary gas, and 0.70 L/min for the carrier gas. Axial exposure conditions and rinse parameters were carefully controlled to ensure measurement accuracy and minimize interferences, thereby ensuring reliable analysis of heavy metals in the samples.

Statistical analysis

The map of the study areas was created using ArcGIS Pro for precise visualization of the capture sites. Statistical tests, including Pearson correlation and principal component analysis (PCA), were performed using Python via Google Colab with the Matplotlib and Seaborn libraries, as well as SPSS version 25. These tools allowed for thorough analysis and rigorous interpretation of the data.

The concentrations of Pb, Cd, and Zn in the blood of 50 house sparrows from the five sites studied in the city of Meknes show significant variations depending on the activity of each site. In general, the distribution of heavy metals follows distinct trends for each metal. The highest concentrations of lead were observed in the industrial zone (IZ) and the Town centre (TC), with average values of 336.02 µg/L and 152.96 µg/L, respectively. In contrast, in the rural area (Ref), lead levels were on average ten times lower than those in the industrial zone. A similar pattern was observed for Cd, where industrial and urban areas showed high concentrations, with averages of 12.28 µg/L for IZ and 19.51 µg/L for TC, while the Ref area had the lowest levels, with an average of 1.83 µg/L. Regarding Zn, the highest concentrations were found in the industrial and rural areas, with averages of 1736.09 µg/L for IZ and 1386.53 µg/L for Ref. Medium traffic areas, such as the Fes-Meknes main road (MR) and the Sidi Said bus station (SS), showed intermediate concentrations, reflecting moderate zinc contamination due to traffic and human activities. Figure 2

The statistical analysis of the data for the three variables (Pb, Cd, and Zn) and 50 individuals (blood of house sparrows) was conducted using Principal Component Analysis (PCA). The correlation matrix of the different elements studied shows a close relationship between the various parameters (Table 1). This relationship is demonstrated by the correlation coefficients.

Table 1

Pearson Correlation Matrix
	Zn (µg/L)	Pb (µg/L)	Cd (µg/L)
Zn (µg/L)	1.000	0.292	0.020
Pb (µg/L)	0.292	1.000	0.418
Cd (µg/L)	0.020	0.418	1.000
The results indicate:

A weak positive correlation between Zn and Pb (0.292), suggesting that these metals may have some common sources but their concentrations are not strongly linked.
An almost negligible correlation between Zn and Cd (0.020), indicating that their sources or mechanisms of accumulation are likely distinct.
A moderate positive correlation between Pb and Cd (0.418), implying that these two metals often co-occur, possibly due to shared sources of pollution such as industrial emissions or traffic.

The results of the PCA show that the first axis (PC1) explains 50.66% of the total inertia of the data, and the second axis (PC2) explains an additional 32.72% (Table 2 and Fig. 3). The projection plane PC1-PC2 shows that the three variables are well represented on the correlation circle (Fig. 4).

Table 2

Correlation between Variables and Principal Components.
	Eeigenvalue	Inertia
PC1	1.520	50.66%
PC2	0.981	32.72%
PC3	0.498	16.62%

The correlation circle shows the relationships between the variables (Zn, Cd, Pb) and the first two principal components (PC1 and PC2) of the principal component analysis (PCA). PC1 explains about 50.7% of the total variance and is mainly influenced by lead (Pb) and cadmium (Cd). PC2 explains about 32.7% of the total variance and is strongly influenced by zinc (Zn). Lead (Pb) is moderately correlated with PC1 and positively with PC2, while cadmium (Cd) is positively correlated with PC1 and negatively with PC2. Zinc (Zn) is strongly correlated with PC2 and very weakly with PC1. This representation shows that Pb moderately influences the first two components, while Zn and Cd have distinct influences on PC1 and PC2, respectively.

The main axis PC1 is strongly correlated with two variables, Pb and Cd (located on the positive side of the component), while the axis PC2 is correlated with Zn (located on the positive side of the component) (Table 3).

Table 3

Correlation between Variables and Principal Components.
	PC1	PC2	PC3
Zn (µg/L)	0.513	0.812	0.278
Pb (µg/L)	0.864	-0.013	-0.504
Cd (µg/L)	0.715	-0.567	0.410

The analysis of the projection of sparrows on the plane formed by the first two principal components (PC1 and PC2), as well as the results of the K-means clustering applied to the same data, is presented in Fig. 5.

The left plot shows each point representing a sampling site, differentiated by colors. Blood samples from sparrows at IZ and TC sites are mainly on the right side of PC1 and the upper side of PC2, indicating higher contamination levels. MR points are in the middle, SS points are in the lower left, and Ref points are on the left side of PC1 and the middle of PC2, indicating lower Pb and Cd but higher Zn levels..

The right plot shows the results of the K-means clustering. The optimal number of clusters was determined using the elbow method, where the sum of squared distances (SSE) was plotted against the number of clusters. The optimal number was chosen where the SSE starts to level off, forming an "elbow" shape, indicating three clusters as the best balance K = 3.

Cluster 0 (red): Sparrows mainly from rural areas (Ref), SS, and MR, with high levels of Zn and low levels of Pb and Cd.
Cluster 1 (blue): Sparrows mainly from industrial zones (IZ) and the city center (TC), as well as some from SS, with low to moderate levels of Zn, Pb, and Cd.
Cluster 2 (green): Sparrows mainly from industrial zones (IZ) and the city center (TC), with high levels of Zn, Pb, and Cd.

Samples from the industrial zone (IZ) and the city center (TC) tend to group in clusters 1 and 2, suggesting similar contamination profiles for lead, cadmium, and zinc. In contrast, samples from the rural site (Ref) stand out, forming a distinct cluster (Cluster 0) with high levels of zinc and low levels of lead and cadmium. These results provide a clear perspective on the spatial distribution of heavy metal pollution in the studied region.

The results of this study show a distinct distribution of heavy metal concentrations (Pb, Cd, Zn) in the blood of house sparrows (Passer domesticus) depending on the urban and rural zones in Meknes. The main observation is that the levels of lead (Pb) and cadmium (Cd) are significantly higher in the industrial zones (IZ) and the town centre (TC) compared to other sites, while zinc (Zn) levels are higher both in the industrial zone and the rural site (Ref).

The elevated levels of Pb and Cd in industrial areas and high-traffic zones highlight the significant impact of anthropogenic activities such as industrial emissions, vehicle exhaust, and the use of lead-based paints. This is consistent with previous studies showing that high-traffic and industrial areas are major sources of heavy metal pollution (Heidari et al., 2021; Yuan & Wang, 2023)

The results show a clear difference between urban and rural areas. Pb and Cd levels are the lowest at the rural site of Agouray (Ref), reflecting less influence from industrial activities and traffic. In contrast, Zn levels are high in both the industrial area and the rural site, which could be explained by natural sources of Zn or specific agricultural practices in rural areas that affect soil Zn pollution (Liu et al., 2021; Baweja et al. 2020). These findings are consistent with previous studies presented in Table 4, even though the bioindicators used in those studies were pigeons (Columba livia), which share similar biological and ecological characteristics with house sparrows, as shown in Capoccia et al. (2018).

The detection of Cd, Pb, and Zn in the blood indicates recent exposure to these metals, as mentioned in Michalczyk et al., (2023) ; Wang et al.(2024) and Bakr et al. (2023) studies. Blood serves as a transport vector for these metals, distributing them to various tissues and organs in the body. The concentration of these metals in the blood can be used as a biomarker to assess environmental exposure. High concentrations of these metals in the blood suggest that individuals have been exposed to environmental sources contaminated with these heavy metals (Michalczyk et al., 2023).

Heavy metals are known for their toxic effects on the physiological systems of birds and potentially on humans. House sparrows, serving as bioindicators, show high concentrations of heavy metals such as lead and cadmium in urban areas, leading to compromised immune function and oxidative stress (Swaileh & Sansur, 2006). Exposure to heavy metals like zinc and copper also affects their physical development and health (Albayrak & Pekgöz, 2021). Environmental heavy metal pollution has been linked to altered reproductive functions in sparrows, impacting testis parameters and hormone levels (Yang et al., 2020). High levels of heavy metals in urban sparrows have also led to anemia-like symptoms and reduced antioxidant capacity, indicating overall poorer health compared to birds from less polluted areas (Li et al., 2021). These impacts on sparrows reflect similar potential risks to human health, demonstrating the importance of these birds as environmental indicators.

Table 4

Comparison of concentraon’s metals with other studies
Location	Pb (µg/L)	Cd (µg/L)	Zn (µg/L)	References
Meknes-Morocco				Present study
Industrial Zone	336.02 ± 141.13	12.28 ± 6.02	1736.09 ± 691.40
Town Centre	152.96 ± 59.65	19.51 ± 8.00	1386.53 ± 585.14
Medium traffic	59.98 ± 31.79	7.46 ± 3.28	1235.03 ± 427.84
Refrence site	10.72 ± 3.97	1.83 ± 0.79	1633.12 ± 514.66
Mohammedia—Morocco				Kouddaneet al. (2016)
Less contaminated area	25.14 ± 6.02	0.89 ± 0.34	6830 ± 937.16
Medium traffic	68.98 ± 22.58	2.48 ± 1	3591.7 ± 1009.18
Centre of town	167.54 ± 31.65	6.2 ± 2.71	2007.6 ± 605.92
Industrial	206.36 ± 34.97	5.97 ± 2.27	2818.3 ± 1146.96
Rabat—Morocco				Elabidi et al. (2010)
Kamra	16.4 ± 1.60	1.58 ± 0.35	3463 ± 256
Centre of town	22.12 ± 2.56	2.24 ± 0.3	4449 ± 398
Oulja	31.33 ± 2.85	1.13 ± 0.3	6998 ± 396
Allal Behraoui	11.17 ± 2.14	0.34 ± 0.04	5608 ± 224
Amsterdam—Netherlands				Schilderman et al. (1997)
High traffic	253 ± 182	5.24 ± 2.48	1680 ± 100
Medium traffic	73.3 ± 18.6	6.20 ± 2.96	2212 ± 289
Maastricht	33.8 ± 30.4	7.58 ± 2.6	1396 ± 282
Assen	26.6 ± 17.9	6.67 ± 2.0	1443 ± 401
London/United Kingdom Chelsea	1011 ± 132			Hutton and Goodman (1980)
Mortlake	452 ± 103
Heathrow	162 ± 55
Controls	190 ± 26

The findings of this study highlight the significant impact of urban pollution on the blood levels of heavy metals in house sparrows in Meknes, Morocco. Industrial and high-traffic areas show elevated concentrations of lead and cadmium, whereas zinc levels are high in both industrial and rural areas. These variations underscore the influence of anthropogenic activities such as industrial emissions and vehicular traffic on environmental contamination. House sparrows, due to their close association with human environments and their sedentary nature, prove to be effective bioindicators of heavy metal pollution. The study's results call for enhanced pollution control measures in high-risk areas to mitigate ecological and health risks. Future research should focus on long-term monitoring and the potential health impacts on both wildlife and human populations in urban environments.

Acknowledgements

We express our gratitude to all those who provided expertise and support throughout this research. Special thanks go to the department and faculty members for their invaluable assistance and to the funding bodies for their financial support.

Author Contributions

Youssef Haddadi drafted the manuscript, interpreted the results, created the location maps, performed the statistical tests, and generated the figures. Abdelkader Chahlaoui provided essential guidance in drafting and revising the manuscript, offering critical and intellectual insights. Aziz Taouraout was responsible for conducting the analyses using Inductively Coupled Plasma Mass Spectrometry (ICP-MS), crucial for the precise measurement of lead concentrations, and played a pivotal role in the statistical analysis of the data, applying advanced techniques to ensure accurate interpretation. Abdelkhalek Belkhiri was instrumental in data collection and presentation, aiding significantly in the organisation and visual representation of the research findings.

Ethical Approval

All ethical standards and guidelines for the humane treatment of animals were strictly adhered to throughout the course of this study, with approval from the High Commission for Water and Forests.

Consent to Participate

Non applicable.

Consent to Publish

All authors consent to the publication of this manuscript.

Funding

Competing Interests

The authors declare no conflict of interest. This research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Availability of Data and Materials

The data used in this study are available from the corresponding author, Youssef Haddadi, upon reasonable request.

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Dynamics of Heavy Metals in the Blood of House Sparrows (Passer domesticus) Across Different Urban Habitats in Meknes, Morocco

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Abstract

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INTRODUCTION

MATERIALS AND METHODS

Sample collection

Ethical Blood Collection and Anesthesia Protocol for House Sparrows

Isoflurane Anesthesia Protocol

Sample analysis

Statistical analysis

RESULTS

DISCUSSION

CONCLUSION

Declarations

References

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