Bats as bioindicators: an introduction

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1 Bats as bioindicators: an introduction Danilo Russo a, b, * and Gareth Jones a a Wildlife Research Unit, Laboratorio di Ecologia Applicata, Sezione di Biologia e Protezione dei Sistemi Agrari e Forestali, Dipartimento di Agraria, Università degli Studi di Napoli Federico II, via Università 100, 80055, Portici (Italy) b School of Biological Sciences, University of Bristol, Bristol (U.K.) * Corresponding author, [email protected] The human population is growing at an alarming pace, currently numbering over 7 billion people, with catastrophic implications for the sustainability of both humans and other organisms on Earth. It has been recently postulated that we are approaching a planetary-scale critical transition leading to a global state shift, with consequences for biota that will be unprecedented (Barnosky et al. 2012). Slowing down the current dramatic loss of biodiversity which if sustained may constitute a Sixth Mass Extinction (Leakey and Lewin, 1996) is challenging, as illustrated by the frustrating failure to halt biodiversity loss by 2010 as targeted by governments worldwide under the Countdown 2010 Declaration. Despite the enormous challenges, there is general consensus agreeing that major moral and practical reasons exist for humankind to reduce the speed of biodiversity loss, and science can provide a major evidence base to at least show the best directions to follow. Bioindicators are key tools to mitigate human impact on biota and to achieve sustainable development declared as a major goal in the 1992 Rio Convention on Biodiversity. Bioindicators offer the potential for assessing ecosystem health state before this is functionally compromised, and allow detection of biological responses on a community scale that can inform policy makers. For example, bats are used as part of a suite of biodiversity indicator species in the UK to assess environmental health. Given these major practical implications, bioindication must be regarded as an important subdiscipline of conservation biology (McGeoch, 1998). A number of definitions of bioindicator can be found in the scientific literature. A broad one is biota that are developed as indicators of the quality of the environment, the biotic component, or 1

2 humans within an ecosystem (Burger 2006). In addition, following McGeoch (1998), three categories of bioindicators may be recognized based on their main field of application, i.e. a) environmental indicators (whose responses to changes in environmental state are predictable, readily observed and quantified); b) ecological indicators (demonstrating the environmental change effects on biotic systems); and 3) surrogate taxa or biodiversity indicators (taxonomic or functional groups whose diversity correlates positively with the overall community diversity in a biotope, ecosystem or region). Therefore, the three categories fulfill separate monitoring goals, regarding respectively environmental change (physical or chemical alterations), ecological processes, and biodiversity (Holt & Miller 2011). Although bioindication requires the selection of organisms or processes exhibiting peculiar characteristics, there are basic properties that should characterize any bioindicator, including ease of sampling and monitoring, a wide distribution corresponding to a range of exposures to a certain stressor, taxonomic stability and contributing to important ecosystem services. Bats are among the most diverse vertebrate groups, with more than 1300 species (Fenton and Simmons, 2014). There is great interest on the potential importance of bats as bioindicators, as these mammals can be reliably monitored and recognized, are taxonomically stable, reactive to environmental stressors and providers of important ecosystem services ranging from pest control to pollination or seed dispersal (Jones et al. 2009; Jones 2012). The high level occupied by insectivorous bats in trophic chains or the tight link with plant communities of pollinators or seed dispersers makes these mammals particularly responsive to habitat changes. Bats are especially sensitive to habitat fragmentation and changes in land use, and in many cases can be valuable indicators of environmental quality more generally. At an international level, the potential application of bats as bioindicators has been highlighted in contexts such as EUROBATS (The Agreement on the Conservation of Populations of European Bats) and BatLife Europe (a European partnership of national bat conservation organizations). However, to better exploit the potential of bats as bioindicators, more research in this field is needed. In fact, after a groundbreaking review on the subject (Jones et al. 2009) and an inspiring workshop held in Granollers in 2012 (Flaquer and Puig-Montserrat 2012) relatively few advances have been made into this exciting field (see e.g. Park, 2015; Ancillotto and Russo, 2015) and most evidence comes from studies aiming to assess the conservation needs of bat species or assemblages rather than from work tailored on testing the potential and performance of bats as bioindicators. The main aim of this Special Issue of Mammalian Biology is to enthuse interest in the scientific community regarding the potential of bats as bioindicators. We present both original studies and 2

3 review papers covering some key aspects of bat natural history with respect to their potential performance in bioindication. Some of the contributions present methodological approaches to bat monitoring in order to track habitat changes or the presence of pollutants. Meyer (2015) highlights some of the main challenges posed by monitoring population- and assemblage-level changes of bats with a special focus on methodology and statistics and remarks that particularly in speciose bat communities such as in the tropics, species turnover and composition, rather than species richness, should be targeted as representative variables to understand anthropogenic changes. Van der Meij et al. (2015) describe the methodology employed to implement a prototype pan-european bat indicator which attracted great media attention recently funded by the European Environmental Agency. Limitations and further developments of the indicator, aimed to unveil population trends on a broad geographical scale from regional trends in hibernation counts, are also discussed. Flache et al. (2015) and Rydell and Russo (2015) present novel approaches to non-invasive monitoring: the former describe the analysis of trace metal concentrations in hairs as a non-invasive and cost-effective way to study toxicity in biological communities, whereas the latter employ camera-trapping at drinking sites to record information about bat species as well as, in several cases, individual characteristics such as sex or reproductive status without catching study subjects. Korine et al. (2015) show that neither total bat activity nor species richness in desert habitats may indicate changes in water chemistry and quality, recommending the use of measuring the activity of specific species as indicators of water quality. Several other papers look at the responses of bats to ecosystem alterations a key property of suitable bioindicators including changes in agricultural practices (Park, 2015), urbanization (Ancillotto and Russo, 2015), light pollution (Stone et al. 2015), heavy metals (Zukal et al. 2015), and drought events (Amorim et al, 2015). Finally a study on soprano pipistrelles Pipistrellus pygmaeus in the rice paddy fields of Catalunia (Puig-Montserrat et al. 2015) shows the importance of this bat s foraging activity to suppress infestations of rice borer moth (Chilo suppressalis), providing a good example of an important ecosystem service provided by bats. Although we are aware that this selection of papers does not cover the entire scope of the importance of bats for bioindication, we hope it represents a further step towards developing and encouraging scientific research in this field to achieve the goal of employing bats to effectively characterize ecosystem health and its changes over time. 3

4 References Amorim, F., Mata, V.A., Beja, P., Rebelo, H., Effects of a drought episode on the reproductive success of European free-tailed bats, Tadarida teniotis. Mammalian Biology. Ancillotto, L., Russo, D., Sensitivity of bats to urbanization: a review. Mammalian Biology, this issue. Barnosky, A.D., Hadly, E.A., Bascompte, J., Berlow, E.L., Brown, J.H., Fortelius, M., Getz, W.M., Harte, J., Hastings, A., Marquet, P.A., Martinez, N.D., Mooers, A., Roopnarine, P., Vermeij, G., Williams, J.W., Gillespie, R., Kitzes, J., Marshall, C., Matzke, N., Mindell, D.P., Revilla, E., Smith, A.B., Approaching a state shift in Earth s biosphere. Nature 486, Burger, J., Bioindicators: types, development, and use in ecological assessment and research. Environmental Bioindicators 1, Fenton, MB & Simmons, NB Bats: a world of science and mystery. University of Chicago Press, Chicago. Flache, L., Becker, N.I., Kierdorf, U., Czamecki, S., Düring, R.-A., Encarnação, J.A, Hair samples as monitoring units for assessing metal exposure of bats: a new tool for risk assessment. Mammalian Biology, this issue. Flaquer, C., Puig-Montserrat, X. (Eds.), Proceedings of the International Symposium on the Importance of Bats as Bioindicators. Museum of Natural Sciences Edicions, Granollers. Holt, E.A., Miller, S.W., Bioindicators: using organisms to measure environmental impacts. Nature Education Knowledge 3, 8. Jones, G., Jacobs, D.S., Kunz, T.H., Willig, M.R., Racey, P.A., 2009 Carpe noctem: the importance of bats as bioindicators. Endangered Species Research 8, Jones, G., What bioindicators are and why they are important. In: Flaquer, C., Puig- Montserrat, X. (Eds). Proceedings of the International Symposium on the Importance of Bats as Bioindicators. Museum of Natural Sciences Edicions, Granollers, pp

5 Korine, C., Adams, A., Shamir, U., Gross, A., Effect of water quality on species richness and activity of desert-dwelling bats. Mammalian Biology, this issue. Leakey, R., Lewin, R., The Sixth Extinction: Biodiversity and its survival. Phoenix, London. McGeoch, M.A., The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews 73, Meyer, C., Methodological challenges in monitoring bat population- and assemblage-level changes for anthropogenic impact assessment. Mammalian Biology, this issue. Park, K., Mitigating the impacts of agriculture on biodiversity: bats and their potential role as bioindicators. Mammalian Biology, this issue. Puig-Montserrat, X., Torre, I., López-Baucells, A., Guerrieri, E., Monti, M., Ràfols-García, R., Ferrer, X., Gisbert, D., Flaquer, C., Pest control service provided by bats in Mediterranean rice paddies: linking agroecosystems structure to ecological functions. Mammalian Biology, this issue. Rydell, J., Russo, D., Photography as a low-impact method to survey bats. Mammalian Biology, this issue. Van der Meij, T., Van Strien, A.J., Haysom, K.A., Dekker, J., Russ, J., Biala, K., Bihari, Z., Jansen, E., Langton, S., Kurali, A., Limpens, H., Meschede, A., Petersons, G., Presetnik, P., Prüger, J., Reiter, G., Rodrigues, L., Schorcht, W., Uhrin, M., Vintulis, V., Return of the bats? A prototype indicator of trends in European bat populations in underground hibernacula. Mammalian Biology, this issue. Zukal, J., Pikula, J., Bandouchova, H., Bats as bioindicators of heavy metal pollution: history and prospect. Mammalian Biology, this issue. 5