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Abstract
The stable carbon and nitrogen isotope composition of animal tissues is commonly used to
trace wildlife diets and analyze food chains. Changes in an animal’s isotopic values over
time are generally assumed to indicate diet shifts or, less frequently, physiological changes.
Although plant isotopic values are known to correlate with climatic seasonality, only a few
studies restricted to aquatic environments have investigated whether temporal isotopic
varia-tion in consumers may also reflect environmental baselines through trophic propagation.
We modeled the monthly variation in carbon and nitrogen isotope values in whole
blood of four insectivorous bat species occupying different foraging niches in southern
Spain. We found a common pattern of isotopic variation independent of feeding habits, with
an overall change as large as or larger than one trophic step. Physiological changes related
to reproduction or to fat deposition prior to hibernation had no effect on isotopic variation,
but juvenile bats had higher δ13C and δ15N values than adults. Aridity was the factor that
best explained isotopic variation: bat blood became enriched in both 13C and 15N after hotter
and/or drier periods. Our study is the first to show that consumers in terrestrial ecosystems
reflect seasonal environmental dynamics in their isotope values. We highlight the danger of
misinterpreting stable isotope data when not accounting for seasonal isotopic baselines in
food web studies. Understanding how environmental seasonality is inte-grated in animals’
isotope values will be crucial for developing reliable methods to use stable isotopes as dietary tracers.
Otros datos de interés poco visibles dentro del artículo.
Este trabajo aporta la segunda cita -creo que mundial, pero seguro que ibérica- de cría invernal de Myotis myotis. La otra es Ibáñez C (1997) Winter reproduction in the greater mouse-eared bat (Myotis myotis) in south Iberia. J. Zool 243: 836–840.
En este nuevo caso se trata de la Cueva del Búho, Villamartín (Cádiz):
Myotis myotis and Miniopterus schreibersii were captured in all-year, mixed-sex colonies in
a natural pit cave in Villamartín, Cádiz (36°48'N, 5°35'W). The cave is located on a hillside at
the interface between agricultural land (irrigated and non-irrigated cereal and sunflower crops)
and natural vegetation of the Cádiz mountain system (Mediterranean shrubs and cork oaks). It
hosts a high bat species diversity (Myotis myotis, M. blythii, M. escalerai, Miniopterus schreibersii,
Rhinolophus euryale, R. hipposideros and R. ferrumequinum) and high bat numbers during
the breeding season (up to 3000 individuals). Cave temperature remains ca. 20–22ºC yearround.
For this reason, the ca. 100–300 individuals (several species) that spend the winter in
the cave do not hibernate and emerge to forage. Some females of M. myotis even reproduce
during winter, outside the normal breeding period for temperate-zone bats in the Northern
Hemisphere (from May to July). This is a very rare phenomenon in temperate bats which has
hitherto only been reported once for Myotis myotis in Spain, in a roost of similar microclimatic
conditions (Ibáñez, 1997)
Acknowledgments
The authors would like to thank Jesús Nogueras for sample preparation and processing, Javier
Juste, Jesús Nogueras, Juan Luis García-Mudarra, Carlos Ruiz, Sandra Coque, Olga Mora,
Laura Gamallo, Laura Ibáñez, Susanne Vogel and Mónica Martínez for their help during sample
collection in the field, and the Zoobotanical Garden of Jerez for permission to sample in
their grounds and for their enthusiastic support. We would also like to thank Keith Hobson for
providing insightful comments on the manuscript.
Ana G. Popa-Lisseanu, A.G., S. Kramer-Schadt, J. Quetglas, A. Delgado-Huertas, D. H.
Kelm, & C. Ibáñez. 2015. Seasonal Variation in Stable Carbon and Nitrogen
Isotope Values of Bats Reflect Environmental Baselines. PLoS ONE 10(2):e0117052. doi:10.1371/journal.pone.0117052.
[La variación estacional en los valores de isótopos estables de Carbono y Nitrógeno de murciélagos reflejan los cambios ambientales basales]
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The stable carbon and nitrogen isotope composition of animal tissues is commonly used to
trace wildlife diets and analyze food chains. Changes in an animal’s isotopic values over
time are generally assumed to indicate diet shifts or, less frequently, physiological changes.
Although plant isotopic values are known to correlate with climatic seasonality, only a few
studies restricted to aquatic environments have investigated whether temporal isotopic
varia-tion in consumers may also reflect environmental baselines through trophic propagation.
We modeled the monthly variation in carbon and nitrogen isotope values in whole
blood of four insectivorous bat species occupying different foraging niches in southern
Spain. We found a common pattern of isotopic variation independent of feeding habits, with
an overall change as large as or larger than one trophic step. Physiological changes related
to reproduction or to fat deposition prior to hibernation had no effect on isotopic variation,
but juvenile bats had higher δ13C and δ15N values than adults. Aridity was the factor that
best explained isotopic variation: bat blood became enriched in both 13C and 15N after hotter
and/or drier periods. Our study is the first to show that consumers in terrestrial ecosystems
reflect seasonal environmental dynamics in their isotope values. We highlight the danger of
misinterpreting stable isotope data when not accounting for seasonal isotopic baselines in
food web studies. Understanding how environmental seasonality is inte-grated in animals’
isotope values will be crucial for developing reliable methods to use stable isotopes as dietary tracers.
Otros datos de interés poco visibles dentro del artículo.
Este trabajo aporta la segunda cita -creo que mundial, pero seguro que ibérica- de cría invernal de Myotis myotis. La otra es Ibáñez C (1997) Winter reproduction in the greater mouse-eared bat (Myotis myotis) in south Iberia. J. Zool 243: 836–840.
En este nuevo caso se trata de la Cueva del Búho, Villamartín (Cádiz):
Myotis myotis and Miniopterus schreibersii were captured in all-year, mixed-sex colonies in
a natural pit cave in Villamartín, Cádiz (36°48'N, 5°35'W). The cave is located on a hillside at
the interface between agricultural land (irrigated and non-irrigated cereal and sunflower crops)
and natural vegetation of the Cádiz mountain system (Mediterranean shrubs and cork oaks). It
hosts a high bat species diversity (Myotis myotis, M. blythii, M. escalerai, Miniopterus schreibersii,
Rhinolophus euryale, R. hipposideros and R. ferrumequinum) and high bat numbers during
the breeding season (up to 3000 individuals). Cave temperature remains ca. 20–22ºC yearround.
For this reason, the ca. 100–300 individuals (several species) that spend the winter in
the cave do not hibernate and emerge to forage. Some females of M. myotis even reproduce
during winter, outside the normal breeding period for temperate-zone bats in the Northern
Hemisphere (from May to July). This is a very rare phenomenon in temperate bats which has
hitherto only been reported once for Myotis myotis in Spain, in a roost of similar microclimatic
conditions (Ibáñez, 1997)
Acknowledgments
The authors would like to thank Jesús Nogueras for sample preparation and processing, Javier
Juste, Jesús Nogueras, Juan Luis García-Mudarra, Carlos Ruiz, Sandra Coque, Olga Mora,
Laura Gamallo, Laura Ibáñez, Susanne Vogel and Mónica Martínez for their help during sample
collection in the field, and the Zoobotanical Garden of Jerez for permission to sample in
their grounds and for their enthusiastic support. We would also like to thank Keith Hobson for
providing insightful comments on the manuscript.
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