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Research | Open Access

Biologging is suspect to cause corneal opacity in two populations of wild living Northern Bald Ibises (Geronticus eremita)

Johannes Fritz1,2( ), Barbara Eberhard1, Corinna Esterer1, Bernhard Goenner1, Daniela Trobe1, Markus Unsoeld1,5, Bernhard Voelkl1,4, Helena Wehner1, Alexandra Scope3
Waldrappteam, LIFE Northern Bald Ibis, 6162, Mutters, Austria
Department of Behavioural and Cognitive Biology, University of Vienna, Vienna, Austria
Veterinary University Vienna, Vienna, Austria
University of Bern, Vetsuisse Faculty, Bern, Switzerland
Bavarian State Collection of Zoology, Munich, Germany
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Abstract

Background

In this paper, we present evidence that biologging is strongly correlated with eye irritation, with sometimes severely impairing effects. A migratory population of the Northern Bald Ibis (Geronticus eremita, NBI) is reintroduced in Europe, in course of a LIFE + project. Since 2014, all individuals have been equipped with GPS-devices. Remote monitoring allows the implementation of focussed measures against major mortality causes.

Methods

Initially all birds carried battery-powered devices, fixed on the lower back of the birds. Since 2016 an increasing amount of birds has been equipped with solar-powered devices, fixed on the upper back, the more sun-exposed position. In 2016, we observed opacity in the cornea of one eye (unilateral corneal opacity; UCO) during a regular health monitoring for the first time.

Results

By 2018, a total of 25 birds were affected by UCO, with varying intensity up to blindness. Clinical examination of the birds revealed no clear cause for the symptoms. However, only birds carrying a device on the upper back were affected (2017 up to 70% of this group). In contrast, none of the birds carrying devices on the lower back ever showed UCO symptoms. This unexpected relationship between tagging and UCO was discovered in 2017. After we took countermeasures by removing the device or repositioning it on the lower back, we observed an immediate reduction of the incidence rate without any new cases reported since January 2019. NBI roost with their head on the back, one eye closely placed to the device if it was positioned on the upper back. Thus, we conclude that the most parsimonious explanation for the symptomatology is either a repetitive slight temperature rise in the corneal tissue due to electromagnetic radiation by the GSM module of the device or a repetitive slight mechanical irritation of the corneal surface. Concrete evidence is missing so far. Meanwhile, cases of UCO were found in another NBI population.

Conclusion

Our observations indicate that further research in the fast-growing field of biologging is urgently needed. The findings question the positioning of devices on the upper back in birds roosting with the head on the back.

Keywords

ReintroductionBlindnessElectromagnetic radiationEndangered bird speciesEye opacityGPS-devicesMechanical irritationSolar-powered

References

 

Al-Khlaiwi T, Meo SA. Association of mobile phone radiation with fatigue, headache, dizziness, tension and sleep disturbance in Saudi population. Saudi Med J. 2004; 25: 732–6.
Google Scholar
 

Amlaner CJ Jr, Ball NJ. A synthesis of sleep in wild birds. Behaviour. 1983; 87: 85–119.
Crossref Google Scholar
 

Bluff LA, Rutz C. A quick guide to video-tracking birds. Biol Lett. 2008; 4: 319–22.
Crossref Google Scholar
 

Bodey TW, Cleasby IR, Bell F, Parr N, Schultz A, Votier SC, et al. A phylogenetically controlled meta-analysis of biologging device effects on birds: Deleterious effects and a call for more standardized reporting of study data. Methods Ecol Evol. 2018; 9: 946–55.
Crossref Google Scholar
 

Bowden CGR, Smith KW, Bekkay MEl, Oubrou W, Aghnaj A, Jimenez-Armesto M. Contribution of research to conservation action for the Northern Bald Ibis Geronticus eremita in Morocco. Bird Conserv Int. 2008; 18: 74–90.
Crossref Google Scholar
 

Bowlin MS, Henningsson P, Muijres FT, Vleugels RHE, Liechti F, Hedenström A. The effects of geolocator drag and weight on the flight ranges of small migrants. Methods Ecol Evol. 2010; 1: 398–402.
Crossref Google Scholar
 

Braga AFB, Moreira SP, Zampieri PR, Bacchin JMG, Mei PR. New processes for the production of solar-grade polycrystalline silicon: A review. Sol Energ Mat Sol C. 2008; 92: 418–24.
Crossref Google Scholar
 

Daniels WMU, Pitout IL, Afullo TJO, Mabandla MV. The effect of electromagnetic radiation in the mobile phone range on the behaviour of the rat. Metab Brain Dis. 2009; 24: 629–41.
Crossref Google Scholar
 

Forouharmajd F, Pourabdian S, Ebrahimi H. Evaluating temperature changes of brain tissue due to induced heating of cell phone waves. Int J Prev Med. 2018; 9: 40.
Crossref Google Scholar
 

Fritz J. Reintroduction of the Northern Bald Ibis in Europe: Illegal hunting in Italy during autumn migration as the main threat. WAZA Mag. 2015; 31.
Google Scholar
 

Fritz J, Kramer R, Hoffmann W, Trobe D, Unsöld M. Back into the wild: establishing a migratory Northern bald ibis Geronticus eremita population in Europe. Int Zoo Yearb. 2017; 51: 107–23.
Crossref Google Scholar
 
Fritz J, Unsoeld M, Voelkl B. Back into European wildlife: the reintroduction of the Northern Bald Ibis (Geronticus eremita). In: Kaufman A, Bashaw M, Maple T, editors. Scientific foundations of zoos and aquariums: their role in conservation and research. Cambridge: Cambridge University Press; 2019. p. 339–66.https://doi.org/10.1017/9781108183147.014
Crossref
 

Fritz J, Unsöld M. Internationaler artenschutz im kontext der IUCN reintroduction guidelines: Argumente zur wiederansiedlung des waldrapps Geronticus eremita in Europa. Vogelwarte. 2015; 53: 157–68.
Google Scholar
 

Hyland GJ. Physics and biology of mobile telephony. Lancet. 2000; 356: 1833–6.
Crossref Google Scholar
 

Kay WP, Naumann DS, Bowen HJ, Withers SJ, Evans BJ, Wilson RP, et al. Minimizing the impact of biologging devices: Using computational fluid dynamics for optimizing tag design and positioning. Methods Ecol Evol. 2019; 10: 1222–333.
Crossref Google Scholar
 

Kays R, Crofoot MC, Jetz W, Wikelski M. Terrestrial animal tracking as an eye on life and planet. Science. 2015; 348: 2478.
Crossref Google Scholar
 
Kesari KK, Siddiqui MH, Meena R, Verma HN, Kumar S. Cell phone radiation exposure on brain and associated biological systems. Indian J Exp Biol. 2013; 51: 187–200. https://www.embase.com/search/results?subaction=viewrecord& from=export& id=L368489607%0Ahttps://nopr.niscair.res.in/bitstream/123456789/16123/1/IJEB 51%283%29 187–200.pdf%0Ahttps://lh.cineca.it/Ccube/openclink.do?sid=EMBASE& sid=EMBASE& issn=00195189& id=doi:& at.
 

Lee A-K, Hong S-E, Kwon J-H, Choi H-D, Cardis E. Mobile phone types and SAR characteristics of the human brain. Phys Med Biol. 2017; 62: 2741–61.
Crossref Google Scholar
 

López JM, Quevedo MA. Northern Bald Ibis Reintroduction program in Andalusia. Proceedings of 4th International Advisory Group for the Northern Bald Ibis (IAGNBI) Meeting Seekirchen, Austria. 2016; 57–67.
Google Scholar
 

Lowerre-Barbieri SK, Kays R, Thorson JT, Wikelski M. The ocean's movescape: fisheries management in the bio-logging decade (2018–2028). ICES J Mar Sci. 2019; 76: 477–88.
Crossref Google Scholar
 

Mailankot M, Kunnath A, Jayalekshmi H, Koduru B, Valsalan R. Radio frequency electromagnetic radiation (RF-EMR) from GSM (09/18GHz) mobile phones induces oxidative stress and reduces sperm motility in rats. Clinics. 2009; 64: 6.
Google Scholar
 

Mellish JA, Thomton J, Horning M. Physiological and behavioral response to intra-abdominal transmitter implantation in Steller sea lions. J Exp Mar Biol Ecol. 2007; 351: 283–93.
Crossref Google Scholar
 
Nagata H, Yamagish S. Re-introduction of crested ibis on Sado Island, Japan. In: Soorae PS, editor. Global re-introduction perspectives: 2013. Further case studies from around the globe. Gland, Switzerland: IUCN/SSC Re-introduction Specialist Group and Abu Dhabi, UAE: Environment Agency-Abu Dhabi; 2013. p. 58–62.
 

O'Donoghue P, Rutz C. Real-time anti-poaching tags could help prevent imminent species extinctions. J Appl Ecol. 2016; 53: 5–10.
Crossref Google Scholar
 

Obrecht H, Pennycuick C, Fuller M. Wind tunnel experiments to assess the effect of back-mountd radio transmitters on birds body drag. J Exp Biol. 1988; 135: 265–73.
Crossref Google Scholar
 

Pauli A, Cruz-Martinez L, Ponder J, Redig P, Glaser A, Klauss G. Ophthalmologic and oculopathologic findings in red-tailed hawks and Cooper's hawks with naturally acquired West Nile virus infection. J Am Vet Med Assoc. 2007; 231: 1240–8.
Crossref Google Scholar
 

Pennycuick CJ, Fast PLF, Ballersta N, Rattenborg N. The effect of an external transmitter on the drag coefficient of a bird's body, and hence on migration range, and energy reserves after migration. J Ornithol. 2012; 153: 633–44.
Crossref Google Scholar
 

Portugal SJ, White CR. Miniaturization of biologgers is not alleviating the 5% rule. Methods Ecol Evol. 2018; 9: 1662–6.
Crossref Google Scholar
 
Pschera A. Das Internet der Tiere. Berlin: Matthes & Seitz Verlag; 2014.https://doi.org/10.1590/S1807-59322009000600011
Crossref
 
Rusnani A, Norsuzila N. Measurement and analysis of temperature rise caused by handheld mobile telephones using infrared thermal imaging. 2008 IEEE International RF and Microwave Conference. 2008. https://doi.org/. https://doi.org/10.1109/RFM.2008.4897449
 

Rutz C, Hays GC. New frontiers in biologging science. Biol Lett. 2009; 5: 289–92.
Crossref Google Scholar
 

Schacter CR, Jones IL. Effects of geolocation tracking devices on behavior, reproductive success, and return rate of Aethia Auklets: an evaluation of tag mass guidelines. Wilson J Ornithol. 2017; 129: 459–68.
Crossref Google Scholar
 

Serra G, Lindsell JA, Peske L, Fritz J, Bowden CGR, Bruschini C, et al. Accounting for the low survival of the Critically Endangered northern bald ibis Geronticus eremita on a major migratory flyway. Oryx. 2014; 49: 312–20.
Crossref Google Scholar
 

Shafahi M, Vafai K. Human eye response to thermal disturbances. J Heat Trans. 2010; 133: 011009.
Crossref Google Scholar
 
Tahvanainen K, Niño J, Halonen P, Kuusela T, Alanko T, Laitinen T, et al. Effects of cellular phone use on ear canal temperature measured by NTC thermistors. Clin Physiol Funct. 2007; I(27): 162–72.https://doi.org/10.1017/S0030605313000665
Crossref
 
Team RC. R: A language and environment for statistical computing. R Foundation for Statistical Computing; 2014. Retrieved from https://www.r-project.org/.https://doi.org/10.1115/1.4002360
Crossref
 

Thaxter CB, Ross-Smith VH, Clark JA, Clark NA, Conway GJ, Masden EA, et al. Contrasting effects of GPS device and harness attachment on adult survival of Lesser Black-backed Gulls Larus fuscus and Great Skuas Stercorarius skua. Ibis. 2016; 158: 279–90.
Crossref Google Scholar
 

Vandenabeele SP, Shepard EL, Grogan A, Wilson RP. When three per cent may not be three per cent; device-equipped seabirds experience variable flight constraints. Mar Biol. 2012; 159: 1–14.
Crossref Google Scholar
 

Vickers M, Hartley W, Mason R, Dubey J, Schollam L. Blindness associated with toxoplasmosis in canaries. J Am Vet Med Assoc. 1992; 200: 1723–5.
Crossref Google Scholar
 

Wai-Yeung W, Cheuk-Lam H. Organometallic photovoltaics: A new and versatile approach for harvesting solar energy using conjugated polymetallaynes. Acc Chem Res. 2010; 43: 1246–56.
Crossref Google Scholar
 

Wascher CAF, Scheiber IBR, Weiß BM, Kotrschal K. Heart rate responses to agonistic encounters in greylag geeseAnser anser. Anim Behav. 2009; 77: 955–61.
Crossref Google Scholar
 

Wikelski M, Kays RW, Kasdin NJ, Thorup K, Smith JA, Swenson GW. Going wild: what a global small-animal tracking system could do for experimental biologists. J Exp Biol. 2007; 210: 181–6.
Crossref Google Scholar
 

Wikelski M, Tertitski G. Ecology: Living sentinels for climate change effects. Science. 2016; 352: 775–6.
Crossref Google Scholar
 

Williams S, Fulton R, Render J, Mansfield L, Bouldin M. Ocular and encephalic toxoplasmosis in canaries. Avian Dis. 2001; 45: 262–7.
Crossref Google Scholar
 

Wirtz S, Boehm C, Fritz J, Kotrschal K, Veith M, Hochkirch A. Optimizing the genetic management of reintroduction projects: genetic population structure of the captive Northern Bald Ibis population. Conserv Genet. 2018; 19: 853–64.
Crossref Google Scholar
 

Wünschmann A, Armién A, Khatri M, Martinez L, Willette M, Glaser A. Ocular lesions in Red-Tailed Hawks (Buteo jamaicensis) with naturally acquired west nile disease. Vet Pathol. 2017; 54: 277–87.
Crossref Google Scholar
 
Ziegelberger G. ICNIRP Statement on the "guidelines for limiting exposure to time-varying electric, magnetic and electromagnetic fields (up to 300 ghz)" ICNIRP Health Physics 2009973257819667809. Health Phys. 2009; 97: 257–8. Retrieved from https://www.icnirp.org/cms/upload/publications/ICNIRPStatementEMF.pdf.
Avian Research
Volume 11 Issue 1,
January 2020
Article number: 38
DOI: 10.1186/s40657-020-00223-8
Cite this article:
Fritz J, Eberhard B, Esterer C, et al. Biologging is suspect to cause corneal opacity in two populations of wild living Northern Bald Ibises (Geronticus eremita). Avian Research, 2020, 11(1): 38. https://doi.org/10.1186/s40657-020-00223-8

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Received: 22 April 2020
Accepted: 24 September 2020
Published: 16 October 2020
© The Author(s) 2020.

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