Journal of Threatened Taxa | www.threatenedtaxa.org | 26 July 2020 | 12(10): 16377–16379

 

 

ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print) 

doi: https://doi.org/10.11609/jott.6225.12.10.16377-16379

#6225 | Received 26 May 2020 | Finally accepted 15 July 2020

 

 

Tracing heavy metals in urban ecosystems through the study of bat guano - a preliminary study from Kerala, India

 

Jithin Johnson 1  & Moncey Vincent 2

 

1,2 Department of Zoology, Sacred Heart College (Autonomous), Pandit Karuppan Road, Thevara, Kerala 682013, India.

1 jithinjohnson94@gmail.com (corresponding author), 2 moncey.vincent@gmail.com

 

 

 

Editor: Paul Racey, University of Exeter, UK.      Date of publication: 26 July 2020 (online & print)

 

Citation: Johnson, J. & M. Vincent (2020). Tracing heavy metals in urban ecosystems through the study of bat guano - a preliminary study from Kerala, India.  Journal of Threatened Taxa 12(10): 16377–16379. https://doi.org/10.11609/jott.6225.12.10.16377-16379

 

Copyright: © Johnson & Vincent 2020. Creative Commons Attribution 4.0 International License.  JoTT allows unrestricted use, reproduction, and distribution of this article in any medium by providing adequate credit to the author(s) and the source of publication.

 

Funding: None.

 

Competing interests: The authors declare no competing interests.

 

Acknowledgements: We thank the principal S.H. College, Thevara for providing the necessary laboratory facilities.  We also thank Dr. Anu Gopinath & Ms. Greeshma, KUFOS, Mr. Jaison, CSIR-CECRI and Dr. Adarsh & the Director, SAIF-STIC, CUSAT, for the help rendered in the analysis of the samples.  We are also indebted to Mr. Tijo K. Joy, Mr. Sreehari Raman and Dr. A. Madhavan (Retd.), Bharata Mata College, Thrikkakara for identifying the bat species.

 

 

 

Heavy metal pollution has greatly increased the mobilisation of metals in the air, water, and soil.  Metals such as arsenic, cadmium, chromium, copper, mercury, manganese, nickel, lead, and tin  are toxic at elevated levels and some even at low concentrations.  As these elements do not decay with time, their emission to the environment is a serious problem.  Bio-indicator organisms like small mammals, particularly bats allow detection of biological responses and provide a tool in assessing the state of ecosystem health (Clark 1981).  Insectivorous bats are considered to be the best bio-indicators as they are exposed to contaminants more directly through invertebrates that may consume soil (Ma & Talmage 2001).  Being the only flying mammal, bats are sensitive to a wide range of environmental stresses to which they respond in predictable ways (Zukal et al. 2015) and thus, are important keystone species in the ecosystem, having enormous potential as biodiversity, ecological, and environmental indicators (Jones et al. 2009).  Their widespread distribution and proximity to humans make them susceptible to contamination through anthropogenic activities.  The potential of bats as bio-indicators of pollution is two-fold: Firstly, exposure to contaminants, including heavy metals, contributes to the decrease in bat populations.  Secondly, levels of the contaminants in bat guano serve as an indicator of the prevalent pollution levels in the surrounding environment.  This study aims to evaluate the pollution levels in two different environments using bats as indicator organisms and it is hypothesized that urban areas would reveal comparatively greater amounts of contaminants than rural areas.

Sampling was carried out in different sites from Ernakulam (Mangalavanam Bird Sanctuary and Tripunithura) and Thrissur (Irinjalakuda) districts of Kerala.  Fresh (whenever possible) and few-days-old guano deposits of bats like Pteropus medius Temminck, 1825, Megaderma spasma (Linnaeus, 1758) and Taphozous melanopogon Temminck, 1841 were collected by placing nets fitted onto PVC frame of size 0.8 × 0.8 m on the floor of the bat’s roosting site and left undisturbed for 4–6 days to allow for sufficient guano deposition.  For sample digestion, a mixture of concentrated nitric acid and perchloric acid (5:1 ratio) was added to 0.5g of dry guano in a Borosil glass beaker; the beaker kept in a heating mantle at 90oC for 1–2 h or until digestion was complete.  After cooling, the sample was diluted to 20ml using distilled water, the contents filtered and transferred to clean Borosil glass vials and then stored at room temperature prior to analysis.  Analysis of the metals was done using the Inductively Coupled Plasma Atomic Emission Spectroscopy (ICP-AES) facility at the Kerala University of Fisheries and Ocean Studies, Panangad. Mercury (Hg) analysis was performed using direct Hg analyser at the Sophisticated Test and Instrumentation Centre, Cochin University of Science and Technology (CUSAT).  Elemental compositions of dry homogenised samples were determined by X-ray fluorescence (XRF) analyser at the CSIR-Central Electrochemical Research Institute, Karaikudi. Statistical analyses was done using the software package PAST v 3.18 and graphs were made using MS Excel.

It has been known that the composition of elements in bat guano normally equals that in the undigested portion of the ingested food, and as such may provide some clues to the location of contaminants in the environment (Martin 1992).  Factors such as the bats’ diet, roosting location, foraging habitat, and metabolism may significantly influence accumulation.  It seems likely, therefore, that heavy metal exposure pathways differ between frugivorous and insectivorous bat species.

Contamination in fruit bats is likely to be through atmospheric pollution, contact with contaminated foliage whilst searching for and eating food, which may be later ingested directly while grooming.  Insectivorous bat species become contaminated mainly through bio-accumulation through the food-chain, i.e., from water/soil/sediments/plants or other sources to insects and finally to the bats themselves.  The additional routes of exposure to heavy metals may include contact with skin and inhalation (Allinson et al. 2006).  Usually, upon oral ingestion, about 5–10% of the metal gets absorbed and about 99.5% of total ingested metal is excreted through faeces/guano thus leaving only 0.5% to be deposited in various body tissues (Klaassen 1976).  Table 1 represents the general composition of elements detected by the XRF analyser in the bat guano used for the study.

Guano analysis indicated the presence of heavy metals such as mercury (Hg) and various other metals in varying concentrations.  The concentration of metals like lead, cadmium and zinc, however, were below detection limits.  Figure 1 represents the concentration of Hg obtained from the direct Hg analyser and Table 2 represent the concentrations of the metals (Chromium, Copper, Manganese and Nickel) obtained using the ICP-AES analyser.

In our study, the concentration of mercury varied between the bats from the urban areas of Ernakulam and the rural areas of Irinjalakuda (Thrissur), with higher contamination levels in the Ernakulam District.  The composition of guano also varied between the insectivorous and frugivorous bats and this was indicated by the presence of the elements Aluminium (Al) and Titanium (Ti) in insectivorous bat guano.  It was also noted that the levels of Copper (Cu), Chromium (Cr), Manganese (Mn), and Nickel (Ni) were significantly different between the insectivores from Ernakulam and those from Irinjalakuda.  This may be probably due to the elevated pollution levels in Ernakulam.  Further studies are needed to determine if these values are representative of the bat colonies from Kerala, to pinpoint the sources of contamination, and to determine if these levels of contamination adversely affect bats.

Variability in the levels of metals found in bat bodies is influenced by their background environmental levels, which in turn reflects the amounts accumulated.  Metals may interfere with the normal functioning of the immune system, cause physiological and histological distress and thus, increase the prevalence of parasites or wildlife infectious diseases (Hernout et al. 2016).  Environmental pollution and contamination, in turn, can cause population declines in bats.  Assessments of these contaminants thus, help us to understand the levels that would harm humans.

As far as we are aware, there are no other time-trend data for heavy metals in bats in Kerala, and so it is impossible to assess whether the trend in the studied bats is typical for other bat species.  Ecotoxicological data are essential for risk assessment and decision-making in bat conservation.  Data from this study provides information on baseline levels of interest to monitor status and trends in the heavy metal residue in the bats of the study areas, and therefore, they represent a tool to evaluate potential wildlife, ecological, and human health exposure.  Such an evaluation of the contaminant load through guano analysis sheds light on the potential use of guano as a simple, relatively inexpensive and non-invasive bio-indicator tool to assess the prevalent pollution levels and thus, the environmental quality.  The relationship between levels of heavy metals in bat guano, prey analysis, and the various components of the environment in which the insects develop, should also prove to be a fruitful area for future research.

 

 

Table 1. Elemental composition of guano from different bats.

Element

Avg. mass (%) (n=4)

T. melanopogon

M. spasma

P. medius (1)

P. medius (2)

Aluminium (Al)

4.6105

5.5846

BDL

BDL

Calcium (Ca)

10.7272

17.0122

21.221

21.1739

Copper (Cu)

BDL

0.4237

1.3149

0.1164

Iron (Fe)

42.8869

15.2537

4.1669

6.8953

Potassium (K)

BDL

3.1887

35.3471

36.4112

Molybdenum (Mo)

0.0001

0.0002

0.0003

0.0002

Oxygen (O)

34.7198

39.3272

27.7743

27.3338

Silicon (Si)

6.7776

16.8635

8.335

7.2244

Titanium (Ti)

0.278

1.1079

BDL

BDL

Zinc (Zn)

BDL

1.2382

1.8369

0.5562

BDL →Below detection limit ≈ 0

(1)→ Irinjalakuda, Thrissur; (2) → Ernakulam

 

 

Table 2. Comparison of metal concentrations (mg/kg wet weight) in the guano of insectivorous bats from Ernakulam and Thrissur (mean ± standard deviation [n=12]).

Metals

Cr

Cu

Mn

Ni

Ernakulam

79.69 ± 35.56

3973.68 ± 418.38

820.12 ± 464.26

60.03 ± 22.23

Thrissur

24.93 ± 10.56

2869.22 ± 503.13

76.92 ± 38.62

24.61 ± 16.68

p-value

0.016

0.057

0.016

0.033

p-values were calculated at 95% confidence using Mann-Whitney U test

 

 

For figure - - click here

 

 

References

 

Clark, D.R., Jr. (1981). Bats and Environmental Contaminants: A Review. USDA Fish and Wildlife Service Special Scientific Report-Wildlife, Washingdon D.C. No. 235.

Ma, W.C. & S. Talmage (2001). Insectivora, pp. 123–158. In: Shore, R.F. & B.A. Rattner (eds.). Ecotoxicology of Wild Mammals. John Wiley & Sons, New York, 752pp.

Jones, G., D.S. Jacobs, T.H. Kunz, M.R. Willig & P.A. Racey (2009). Carpe noctem: the importance of bats as bioindicators. Endangered Species Research 8: 93–115. https://doi.org/10.3354/esr00182

Martin, D.B. (1992). Contaminant studies on endangered bats in northeastern Oklahoma. U.S. Fish and Wildlife Service report, Ecological Services, Tulsa, Oklahoma, 16pp.

Allinson, G., C. Mispagel, N. Kajiwara, Y. Anan, J. Hashimoto, L. Laurenson, M. Allinson & S. Tanabe (2006). Organochlorine and trace metal residues in adult Southern Bent-wing Bat (Miniopterus schreibersiibassanii) in southern Australia. Chemosphere 64: 1464–1471. https://doi.org/10.1016/j.chemosphere.2005.12.067

Klaassen, C.D. (1976). Biliary excretion of metals. Drug Metabolism Reviews 5: 165–196.

Hernout, B.V., C.J. McClean, K.E. Arnold, M. Walls, M. Baxter & A.B.A. Boxall (2016). Fur: a non-invasive approach to monitor metal exposure in bats. Chemosphere 147: 376–381. https://doi.org/10.1016/j.chemosphere.2015.12.104

Zukal, J., J. Pikula & H. Bandouchova (2015). Bats as bioindicators of heavy metal pollution: history and prospect. Mammalian Biology 80: 220–227.