Bats as bioindicators: an introduction

Bats as bioindicators: an introduction
Danilo Russoa, b, * and Gareth Jonesa
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, danrusso@unina.it
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
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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
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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.
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References
Amorim, F., Mata, V.A., Beja, P., Rebelo, H., 2015. Effects of a drought episode on the
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Ancillotto, L., Russo, D., 2015. Sensitivity of bats to urbanization: a review. Mammalian Biology,
this issue.
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Flache, L., Becker, N.I., Kierdorf, U., Czamecki, S., Düring, R.-A., Encarnação, J.A, 2015. Hair
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Ferrer, X., Gisbert, D., Flaquer, C., 2015. Pest control service provided by bats in Mediterranean
rice paddies: linking agroecosystems structure to ecological functions. Mammalian Biology, this
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Rydell, J., Russo, D., 2015. Photography as a low-impact method to survey bats. Mammalian
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Van der Meij, T., Van Strien, A.J., Haysom, K.A., Dekker, J., Russ, J., Biala, K., Bihari, Z., Jansen,
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Zukal, J., Pikula, J., Bandouchova, H., 2015. Bats as bioindicators of heavy metal pollution: history
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