Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Climatic correlates of migrant Natal long-fingered bat (Miniopterus natalensis) phenology in north-eastern South Africa

Mariëtte Pretorius A , Hugh Broders B , Ernest Seamark C and Mark Keith https://orcid.org/0000-0001-7179-9989 A D
+ Author Affiliations
- Author Affiliations

A Mammal Research Institute, Faculty of Natural and Agricultural Sciences, University of Pretoria, Hatfield 0028, Private Bag x20, South Africa.

B Department of Biology, University of Waterloo, 200 University Avenue West, Waterloo, Ontario, N2 L 3G1, Canada.

C AfricanBats NPC, 357 Botha Avenue, Kloofsig, 0157, South Africa.

D Corresponding author. Email: mark.keith@up.ac.za

Wildlife Research 47(5) 404-414 https://doi.org/10.1071/WR19165
Submitted: 12 September 2019  Accepted: 25 February 2020   Published: 12 June 2020

Abstract

Context: For migratory animals, particularly those with long generation times, changing weather patterns may cause a mismatch between periods of expected and actual resource availability, termed phenological mismatch. The cave-dwelling Natal long-fingered bat (Miniopterus natalensis) is a regional migrant within South Africa for which the (hitherto unknown) phenology of migration may be affected by climate.

Aims: To investigate the migration phenology of the Natal long-fingered bat in relation to climate at a maternity cave in South Africa.

Methods: Five years (2014–18) of echolocation data from a maternity cave site in Limpopo, South Africa, were studied. Separate stepwise General Linear Models (GLMs) were constructed for each season using photoperiod, minimum temperature, dew point, rainfall, barometric pressure, humidity and maximum wind speed. Arrival and departure dates among years were also compared.

Key results: Photoperiod had the greatest effect on the magnitude of Natal long-fingered bat phenological patterns in activity across all seasons. Although spring (September - November) arrival at the maternity site was variable across years, summer departure dates did not differ, resulting in a shorter breeding period in the 2017–18 sample year. During the 2016–17 sample year, the magnitude of Natal long-fingered bat activity was significantly lower than in other years, which coincided with El Niño-induced drought conditions and likely impacted resources and led to a reduction in activity and population size.

Conclusions: Photoperiod is a strong predictive cue of the phenology of migration of the Natal long-fingered bat and likely cues migration for this species. The narrow departure dates of these bats from the maternity site supports these results.

Implications: The present study indicates that Natal long-fingered bats use photoperiod as a migration cue and do not appear to shift their spring–summer breeding season, likely making them vulnerable to phenological mismatch and population decline. The research highlights the need for systematic population monitoring for the Natal long-fingered bat.

Additional keywords: activity, bat, phenology, photoperiod, reproduction.


References

Adams, A. M. (2013). Assessing and analyzing bat activity with acoustic monitoring: challenges and interpretations. Ph.D. Thesis, The University of Western Ontario, London, ON, USA.

Adams, A. M., and Fenton, M. B. (2017). Identifying peaks in bat activity: a new application of SaTScan’s space-time scan statistic. Wildlife Research 44, 392–399.
Identifying peaks in bat activity: a new application of SaTScan’s space-time scan statistic.Crossref | GoogleScholarGoogle Scholar |

Adams, A. M., McGuire, L. P., Hooton, L. A., and Fenton, M. B. (2015). How high is high? Using percentile thresholds to identify peak bat activity. Canadian Journal of Zoology 93, 307–313.
How high is high? Using percentile thresholds to identify peak bat activity.Crossref | GoogleScholarGoogle Scholar |

Agafonkin, V. (2018). suncalc: Compute sun position, sunlight phases, moon position and lunar phase. R package version 1.6.9. Available at https://CRAN.R-project.org/package=suncalc [verified 16 May 2019].

Bartoń, K. (2019). MuMIn: Multi-model inference. R package version 1.43.6. Available at https://CRAN.R-project.org/package=MuMIn [verified 7 June 2019]

Bauer, S., Nolet, B. A., Giske, J., Chapman, J. W., Åkesson, S., Hedenström, A., and Fryxell, J. M. (2011). Cues and decision rules in animal migration. In ‘Animal Migration: A Synthesis’. (Eds E. J. Milner-Gulland, J. M. Fryxell, and A. R. E. Sinclair.) pp. 68–87. (Oxford University Press: Oxford, UK.)

Becker, N., Encarnacao, J., Tschapka, M., and Kalko, E. (2013). Energetics and life-history of bats in comparison to small mammals. Ecological Research 28, 249–258.
Energetics and life-history of bats in comparison to small mammals.Crossref | GoogleScholarGoogle Scholar |

Bender, M. J., and Hartman, G. D. (2015). Bat activity increases with barometric pressure and temperature during autumn in central Georgia. Southeastern Naturalist (Steuben, ME) 14, 231–242.
Bat activity increases with barometric pressure and temperature during autumn in central Georgia.Crossref | GoogleScholarGoogle Scholar |

Benkenstein, A. (2017). ‘Climate Change Adaptation Readiness: Lessons from the 2015/2016 El Niño for Climate Readiness in Southern Africa.’ SAIIA Occasional Paper 250. pp. 1–18. (South African Institute of International Affairs: Johannesburg, South Africa.)

Berková, H., and Zukal, J. (2010). Cave visitation by temperate zone bats: effects of climatic factors. Journal of Zoology 280, 387–395.
Cave visitation by temperate zone bats: effects of climatic factors.Crossref | GoogleScholarGoogle Scholar |

Bowlin, M. S., Bisson, I.-A., Shamoun-Baranes, J., Reichard, J. D., Sapir, N., Marra, P. P., Kunz, T. H., Wilcove, D. S., Hedenström, A., Guglielmo, C. G., Åkesson, S., Ramenofsky, M., and Wikelski, M. (2010). Grand challenges in migration biology. Integrative and Comparative Biology 50, 261–279.
Grand challenges in migration biology.Crossref | GoogleScholarGoogle Scholar | 21558203PubMed |

Brigham, R., Kalko, E., Jones, G., Parsons, S., and Limpens, H. (2004). ‘Bat Echolocation Research: Tools, Techniques and Analysis.’ (Bat Conservation International: Austin, TX, USA.)

Brown, M. E., de Beurs, K., and Vrieling, A. (2010). The response of African land surface phenology to large scale climate oscillations. Remote Sensing of Environment 114, 2286–2296.
The response of African land surface phenology to large scale climate oscillations.Crossref | GoogleScholarGoogle Scholar |

Burnham, K. P., and Anderson, D. R. (2002). ‘Model Selection and Multimodel Inference: a Practical Information-theoretic Approach.’ (Springer Science & Business Media: New York.)

Burnham, K. P., Anderson, D. R., and Huyvaert, K. P. (2011). AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behavioral Ecology and Sociobiology 65, 23–35.
AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons.Crossref | GoogleScholarGoogle Scholar |

Canale, C. I., and Henry, P. (2010). Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Climate Research 43, 135–147.
Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability.Crossref | GoogleScholarGoogle Scholar |

Chambers, L. E., Altwegg, R., Barbraud, C., Barnard, P., Beaumont, L. J., Crawford, R. J. M., Durant, J. M., Hughes, L., Keatley, M. R., Low, M., Morellato, P. C., Poloczanska, E. S., Ruoppolo, V., Vanstreels, R. E. T., Woehler, E. J., and Wolfaardt, A. C. (2013). Phenological changes in the southern hemisphere. PLoS One 8, e75514.
Phenological changes in the southern hemisphere.Crossref | GoogleScholarGoogle Scholar | 24098389PubMed |

Cook, C., Reason, C. J., and Hewitson, B. C. (2004). Wet and dry spells within particularly wet and dry summers in the South African summer rainfall region. Climate Research 26, 17–31.
Wet and dry spells within particularly wet and dry summers in the South African summer rainfall region.Crossref | GoogleScholarGoogle Scholar |

Corben, C. (2017). AnalookW for bat call analysis using ZCA. Version 4.2n. Available at https://www.titley-scientific.com/downloads-support/firmware-software [verified 10 April 2018].

Crawley, M. J. (2012). ‘The R book.’ (John Wiley & Sons: Chichester.)

Cumming, G., and Bernard, R. (1997). Rainfall, food abundance and timing of parturition in African bats. Oecologia 111, 309–317.
Rainfall, food abundance and timing of parturition in African bats.Crossref | GoogleScholarGoogle Scholar | 28308124PubMed |

Dechmann, D. K., Wikelski, M., Ellis-Soto, D., Safi, K., and O’Mara, M. T. (2017). Determinants of spring migration departure decision in a bat. Biology Letters 13, 20170395.
Determinants of spring migration departure decision in a bat.Crossref | GoogleScholarGoogle Scholar | 28931730PubMed |

Dingle, H. (2014). ‘Migration: the Biology of Life on the Move.’ (Oxford University Press: New York.)

Erickson, J. L., and West, S. D. (2002). The influence of regional climate and nightly weather conditions on activity patterns of insectivorous bats. Acta Chiropterologica 4, 17–24.
The influence of regional climate and nightly weather conditions on activity patterns of insectivorous bats.Crossref | GoogleScholarGoogle Scholar |

Fleming, T. H., and Eby, P. (2003). Ecology of bat migration. In ‘Bat Ecology’. (Eds T. H. Kunz, and M. B. Fenton.) pp. 164–65. (The University of Chicago Press: Chicago, IL, USA.)

Ford, W. M., Britzke, E. R., Dobony, C. A., Rodrigue, J. L., and Johnson, J. B. (2011). Patterns of acoustical activity of bats prior to and following white-nose syndrome occurrence. Journal of Fish and Wildlife Management 2, 125–134.
Patterns of acoustical activity of bats prior to and following white-nose syndrome occurrence.Crossref | GoogleScholarGoogle Scholar |

Fournier, F., Pelletier, D., Vigneault, C., Goyette, B., and Boivin, G. (2005). Effect of barometric pressure on flight initiation by Trichogramma pretiosum and Trichogramma evanescens (Hymenoptera: Trichogrammatidae). Environmental Entomology 34, 1534–1540.
Effect of barometric pressure on flight initiation by Trichogramma pretiosum and Trichogramma evanescens (Hymenoptera: Trichogrammatidae).Crossref | GoogleScholarGoogle Scholar |

Fox, J., and Weisberg, S. (2011). ‘An R Companion to Applied Regression.’ (Sage: Thousand Oaks, CA, USA.) Available at https://r-forge.r-project.org/R/?group_id=531 [verified 22 May 2019].

Fristoe, T. S., Burger, J. R., Balk, M. A., Khaliq, I., Hof, C., and Brown, J. H. (2015). Metabolic heat production and thermal conductance are mass-independent adaptations to thermal environment in birds and mammals. Proceedings of the National Academy of Sciences of the United States of America 112, 15934–15939.
Metabolic heat production and thermal conductance are mass-independent adaptations to thermal environment in birds and mammals.Crossref | GoogleScholarGoogle Scholar | 26668359PubMed |

Gienapp, P., Leimu, R., and Merilä, J. (2007). Responses to climate change in avian migration time- microevolution versus phenotypic plasticity. Climate Research 35, 25–35.
Responses to climate change in avian migration time- microevolution versus phenotypic plasticity.Crossref | GoogleScholarGoogle Scholar |

Giraudoux, P. (2019). pgirmess: Spatial analysis and data mining for field ecologists. R package version 1.6.9. Available at https://CRAN.R-project.org/package=pgirmess [verified 22 May 2019].

Guenther, A., and Trillmich, F. (2013). Photoperiod influences the behavioral and physiological phenotype during ontogeny. Behavioral Ecology 24, 402–411.
Photoperiod influences the behavioral and physiological phenotype during ontogeny.Crossref | GoogleScholarGoogle Scholar |

Gwinner, E., and Helm, B. (2003). Circannual and circadian contributions to the timing of avian migration. In ‘Avian Migration’. (Eds P. Berthold, E. Gwinner and E. Sonnenschein.) pp. 81–95. (Springer: Berlin.)

Hamner, K. C. (1940). Interrelation of light and darkness in photoperiodic induction. Botanical Gazette 101, 658–687.
Interrelation of light and darkness in photoperiodic induction.Crossref | GoogleScholarGoogle Scholar |

Jonasson, K. A. (2017). The effects of sex, energy, and environmental conditions on the movement ecology of migratory bats. Ph.D. Thesis, The University of Western Ontario, London, ON, USA.

Kassambara, A. (2018). ggpubr: ‘ggplot2’ based publication ready. R package version 0.2. Available at https://CRAN.R-project.org/package=ggpubr [verified 22 May 2019].

Koehler, C. E., and Barclay, R. M. R. (2000). Post-natal growth and breeding biology of the hoary bat (Lasiurus cinereus). Journal of Mammalogy 81, 234–244.
Post-natal growth and breeding biology of the hoary bat (Lasiurus cinereus).Crossref | GoogleScholarGoogle Scholar |

Krzywinski, M., and Altman, N. (2014). Points of significance: visualizing samples with box plots. Nature Methods 11, 119–120.
Points of significance: visualizing samples with box plots.Crossref | GoogleScholarGoogle Scholar | 24645192PubMed |

Kudo, G., and Ida, T. Y. (2013). Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology 94, 2311–2320.
Early onset of spring increases the phenological mismatch between plants and pollinators.Crossref | GoogleScholarGoogle Scholar | 24358716PubMed |

Kunz, T. H., Braun de Torrez, E., Bauer, D., Lobova, T., and Fleming, T. H. (2011). Ecosystem services provided by bats. Annals of the New York Academy of Sciences 1223, 1–38.
Ecosystem services provided by bats.Crossref | GoogleScholarGoogle Scholar | 21449963PubMed |

Lima, C. S., and Fabián, M. E. (2016). Reproductive biology of Artibeus fimbriatus Gray 1838 (Chiroptera) at the southern limit of its geographic range. Biota Neotropica 16, e20160231.
Reproductive biology of Artibeus fimbriatus Gray 1838 (Chiroptera) at the southern limit of its geographic range.Crossref | GoogleScholarGoogle Scholar |

Linton, D. M. (2009). Bat ecology & conservation in lowland farmland. Ph.D. Thesis, University of Oxford, Oxford, UK.

Linton, D. M., and Macdonald, D. W. (2018). Spring weather conditions influence breeding phenology and reproductive success in sympatric bat populations. Journal of Animal Ecology 87, 1080–1090.
Spring weather conditions influence breeding phenology and reproductive success in sympatric bat populations.Crossref | GoogleScholarGoogle Scholar | 29635800PubMed |

Lüdecke, D. (2019). sjPlot: Data visualization for statistics in social science. R package version 2.6.3. Available at https://CRAN.R-project.org/package=sjPlot [verified 5 June 2019].

MacMynowski, D. P., and Root, T. L. (2007). Climate and the complexity of migratory phenology: sexes, migratory distance, and arrival distributions. International Journal of Biometeorology 51, 361–373.
Climate and the complexity of migratory phenology: sexes, migratory distance, and arrival distributions.Crossref | GoogleScholarGoogle Scholar | 17245563PubMed |

Marra, P. P., Hunter, D., and Perrault, A. M. (2011). Migratory connectivity and the conservation of migratory animals. Environmental Law 41, 317–354.

McGuire, L. P., and Boyle, W. A. (2013). Altitudinal migration in bats: evidence, patterns, and drivers. Biological Reviews of the Cambridge Philosophical Society 88, 767–786.
Altitudinal migration in bats: evidence, patterns, and drivers.Crossref | GoogleScholarGoogle Scholar | 23480862PubMed |

Menzel, A. (2002). Phenology: its importance to the global change community. Climatic Change 54, 379–385.
Phenology: its importance to the global change community.Crossref | GoogleScholarGoogle Scholar |

Meyer, C. F., Schwarz, C. J., and Fahr, J. (2004). Activity patterns and habitat preferences of insectivorous bats in a West African forest–savanna mosaic. Journal of Tropical Ecology 20, 397–407.
Activity patterns and habitat preferences of insectivorous bats in a West African forest–savanna mosaic.Crossref | GoogleScholarGoogle Scholar |

Meyer, G. A., Senulis, J. A., and Reinartz, J. A. (2016). Effects of temperature and availability of insect prey on bat emergence from hibernation in spring. Journal of Mammalogy 97, 1623–1633.
Effects of temperature and availability of insect prey on bat emergence from hibernation in spring.Crossref | GoogleScholarGoogle Scholar |

Miller, B. W. (2001). A method for determining relative activity of free flying bats using a new activity index for acoustic monitoring. Acta Chiropterologica 3, 93–105.

Miller-Butterworth, C. M., Jacobs, D. S., and Harley, E. H. (2003). Strong population substructure is correlated with morphology and ecology in a migratory bat. Nature 424, 187–191.
Strong population substructure is correlated with morphology and ecology in a migratory bat.Crossref | GoogleScholarGoogle Scholar | 12853955PubMed |

Miller-Butterworth, C. M., Eick, G., Jacobs, D. S., Schoeman, M. C., and Harley, E. H. (2005). Genetic and phenotypic differences between South African long-fingered bats, with a global miniopterine phylogeny. Journal of Mammalogy 86, 1121–1135.
Genetic and phenotypic differences between South African long-fingered bats, with a global miniopterine phylogeny.Crossref | GoogleScholarGoogle Scholar |

Mills, M., and Hes, L. (1997). Family Vespertilionidae. In ‘The Complete Book of Southern African Mammals’. (Eds M. Mills, and L. Hes.) pp. 81–82. (Struik Publishers: Cape Town, South Africa.)

Milne, D. J., Fisher, A., Rainey, I., and Pavey, C. R. (2005). Temporal patterns of bats in the top end of the Northern Territory, Australia. Journal of Mammalogy 86, 909–920.
Temporal patterns of bats in the top end of the Northern Territory, Australia.Crossref | GoogleScholarGoogle Scholar |

Møller, A. P., Rubolini, D., and Lehikoinen, E. (2008). Populations of migratory bird species that did not show a phenological response to climate change are declining. Proceedings of the National Academy of Sciences of the United States of America 105, 16195–16200.
Populations of migratory bird species that did not show a phenological response to climate change are declining.Crossref | GoogleScholarGoogle Scholar | 18849475PubMed |

Monadjem, A., Griffin, M., Cotterill, F., Jacobs, D., and Taylor, P. J. (2017). Miniopterus natalensis. The IUCN Red List of Threatened Species. e.T44862A22073129.

Morellato, P. L. C., Talora, D. C., Takahasi, A., Bencke, C. C., Romera, E. C., and Zipparro, V. B. (2000). Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32, 811–823.
Phenology of Atlantic rain forest trees: a comparative study.Crossref | GoogleScholarGoogle Scholar |

Mucina, L., and Rutherford, M. C. (2006). ‘The Vegetation of South Africa, Lesotho and Swaziland.’ (South African National Biodiversity Institute: Pretoria, South Africa.)

Newbould, S. (2003). ‘The Tourism Blueprint Reference Guide to the Nine Provinces of South Africa & including Lesotho and Swaziland.’ (Milnerton Publishing: Cape Town, South Africa.)

O’Brien, R. M. (2007). A caution regarding rules of thumb for variance inflation factors. Quality & Quantity 41, 673–690.
A caution regarding rules of thumb for variance inflation factors.Crossref | GoogleScholarGoogle Scholar |

O’Shea, T. J., and Bogan, M. A. (2003). Monitoring trends in bat populations of the United States and territories: problems and prospects. Information and Technology Report USGS/BRD/ITR–2003-0003. US Geological Survey, Reston, VA, USA.

Paige, K. N. (1995). Bats and barometric pressure: conserving limited energy and tracking insects from the roost. Functional Ecology 9, 463–467.
Bats and barometric pressure: conserving limited energy and tracking insects from the roost.Crossref | GoogleScholarGoogle Scholar |

Parmesan, C., and Matthews, J. (2006). Biological impacts of climate change. In ‘Principles of Conservation Biology’. (Eds M. J. Groom, G. K. Meffe, and C. R. Carroll.) pp. 333–374. (Sinauer Associates. Sunderland, MA, USA.)

Pettit, J. L., and O’Keefe, J. M. (2017). Day of year, temperature, wind, and precipitation predict timing of bat migration. Journal of Mammalogy 98, 1236–1248.

Popa-Lisseanu, A. G., and Voigt, C. C. (2009). Bats on the move. Journal of Mammalogy 90, 1283–1289.
Bats on the move.Crossref | GoogleScholarGoogle Scholar |

Post, E., Pedersen, C., Wilmers, C. C., and Forchhammer, M. C. (2008). Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores. Proceedings. Biological Sciences 275, 2005–2013.
Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores.Crossref | GoogleScholarGoogle Scholar | 18495618PubMed |

Pretorius, M. E., Kearney, T. C., Keith, M., Markotter, W., Seamark, E. C. J. S., and Broders, H. (2019). Increased body mass supports energy compensation theory in the breeding female Natal long-fingered bat Miniopterus natalensis. Acta Chiropterologica 20, 319–328.
Increased body mass supports energy compensation theory in the breeding female Natal long-fingered bat Miniopterus natalensis.Crossref | GoogleScholarGoogle Scholar |

Racey, P. A., and Entwistle, A. C. (2000). Life-history and reproductive strategies of bats. In ‘Reproductive Biology of Bats’. (Eds E. G. Crichton, and P. H. Krutzsch.) pp. 363–414. (Academic Press: London, UK.)

Racey, P. A., and Speakman, J. R. (1987). The energy costs of pregnancy and lactation in heterothermic bats. In ‘Reproductive Energetics in Mammals’. (Eds A. S. I. Loudon, and P. A. Racey.) Symposia of the Zoological Society of London, no 57. pp. 107–125. (The Zoological Society: London, UK.)

R Core Team (2014). R: A Language and Environment for Statistical Computing. Available at https://www.r-project.org/ [verified 1 May 2019].

Renner, S. S., and Zohner, C. M. (2018). Climate change and phenological mismatch in trophic interactions among plants, insects, and vertebrates. Annual Review of Ecology Evolution and Systematics 49, 165–182.
Climate change and phenological mismatch in trophic interactions among plants, insects, and vertebrates.Crossref | GoogleScholarGoogle Scholar |

Roberts, R. M. (1978). Seasonal strategies in insects. New Zealand Entomologist 6, 350–356.
Seasonal strategies in insects.Crossref | GoogleScholarGoogle Scholar |

Rodrigues, L., and Palmeirim, J. (2008). Migratory behaviour of the Schreiber’s bat: when, where and why do cave bats migrate in a Mediterranean region? Journal of Zoology 274, 116–125.
Migratory behaviour of the Schreiber’s bat: when, where and why do cave bats migrate in a Mediterranean region?Crossref | GoogleScholarGoogle Scholar |

Rosenzweig, C., Karoly, D., Vicarelli, M., Neofotis, P., Wu, Q., Casassa, G., Menzel, A., Root, T. L., Estrella, N., Seguin, B., Tryjanowski, P., Liu, C., Rawlins, S., and Imeson, A. (2008). Attributing physical and biological impacts to anthropogenic climate change. Nature 453, 353–357.
Attributing physical and biological impacts to anthropogenic climate change.Crossref | GoogleScholarGoogle Scholar | 18480817PubMed |

Sheather, S. (2009). ‘A Modern Approach to Regression with R.’ (Springer Science & Business Media: New York.)

Sheffield, S. R., Shaw, J. H., Heidt, G. A., and McClenaghan, L. R. (1992). Guidelines for the protection of bat roosts. Journal of Mammalogy 73, 707–710.

Smith, A. D., and McWilliams, S. R. (2016). Bat activity during autumn relates to atmospheric conditions: implications for coastal wind energy development. Journal of Mammalogy 97, 1565–1577.
Bat activity during autumn relates to atmospheric conditions: implications for coastal wind energy development.Crossref | GoogleScholarGoogle Scholar |

South African Weather Service (2018). How are the dates of the four seasons worked out? Available at https://www.weathersa.co.za/home/weatherques [verified 30 March 2020].

Stige, L. C., Stave, J., Chan, K.-S., Ciannelli, L., Pettorelli, N., Glantz, M., Herren, H. R., and Stenseth, N. C. (2006). The effect of climate variation on agro-pastoral production in Africa. Proceedings of the National Academy of Sciences of the United States of America 103, 3049–3053.
The effect of climate variation on agro-pastoral production in Africa.Crossref | GoogleScholarGoogle Scholar | 16492727PubMed |

Swain, J. A. (2016). Impact of temperature and relative humidity on the eye-spotted bud moth, Spilonota ocellana (Lepidoptera: Tortricidae): a climate change perspective. M.Sc. Thesis, Simon Fraser University, Burnaby, BC, USA.

Taylor, C. M., Laughlin, A. J., and Hall, R. J. (2016). The response of migratory populations to phenological change: a migratory flow network modelling approach. Journal of Animal Ecology 85, 648–659.
The response of migratory populations to phenological change: a migratory flow network modelling approach.Crossref | GoogleScholarGoogle Scholar | 26782029PubMed |

Thornton, P. K., Ericksen, P. J., Herrero, M., and Challinor, A. J. (2014). Climate variability and vulnerability to climate change: a review. Global Change Biology 20, 3313–3328.
Climate variability and vulnerability to climate change: a review.Crossref | GoogleScholarGoogle Scholar | 24668802PubMed |

Tøttrup, A. P., Klaassen, R., Kristensen, M. W., Strandberg, R., Vardanis, Y., Lindström, Å., Rahbek, C., Alerstam, T., and Thorup, K. (2012). Drought in Africa caused delayed arrival of European songbirds. Science 338, 1307.
Drought in Africa caused delayed arrival of European songbirds.Crossref | GoogleScholarGoogle Scholar | 23224549PubMed |

Van der Merwe, M. (1973). Aspects of temperature and humidity in preferred hibernation sites of the Natal clinging bat Miniopterus schreibersi natalensis (A. Smith, 1834). African Zoology 8, 121–134.
Aspects of temperature and humidity in preferred hibernation sites of the Natal clinging bat Miniopterus schreibersi natalensis (A. Smith, 1834).Crossref | GoogleScholarGoogle Scholar |

Van der Merwe, M. (1975). Preliminary study on the annual movements of the Natal clinging bat. South African Journal of Science 71, 237–241.

Van der Merwe, M. (1987). Other bat species in maternity caves occupied by Miniopterus schreibersii natalensis. South African Journal of Wildlife 17, 25–27.

Visser, M. E. (2008). Keeping up with a warming world; assessing the rate of adaptation to climate change. Proceedings of the Royal Society B: Biological Sciences 275, 649–659.
Keeping up with a warming world; assessing the rate of adaptation to climate change.Crossref | GoogleScholarGoogle Scholar | 18211875PubMed |

Voigt, C. C., Schneeberger, K., Voigt-Heucke, S. L., and Lewanzik, D. (2011). Rain increases the energy cost of bat flight. Biology Letters 7, 793–795.
Rain increases the energy cost of bat flight.Crossref | GoogleScholarGoogle Scholar | 21543394PubMed |

Voigt, C. C., Rosner, E., Guglielmo, C. G., and Currie, S. E. (2019). Fatty acid profiles of the European migratory common noctule bat (Nyctalus noctula). Naturwissenschaften 106, 33.
Fatty acid profiles of the European migratory common noctule bat (Nyctalus noctula).Crossref | GoogleScholarGoogle Scholar | 31201542PubMed |

Wickham, H. (2009). ggplot2: Elegant graphics for data analysis. Available at https://ggplot2.tidyverse.org [verified 22 May 2019].

Yela, J. L., and Holyoak, M. (1997). Effects of moonlight and meteorological factors on light and bait trap catches of noctuid moths (Lepidoptera: Noctuidae). Environmental Entomology 26, 1283–1290.
Effects of moonlight and meteorological factors on light and bait trap catches of noctuid moths (Lepidoptera: Noctuidae).Crossref | GoogleScholarGoogle Scholar |

Yin, J., Overpeck, J., Peyser, C., and Stouffer, R. (2018). Big jump of record warm global mean surface temperature in 2014–2016 related to unusually large oceanic heat releases. Geophysical Research Letters 45, 1069–1078.
Big jump of record warm global mean surface temperature in 2014–2016 related to unusually large oceanic heat releases.Crossref | GoogleScholarGoogle Scholar |

Zhai, P., Yu, R., Guo, Y., Li, Q., Ren, X., Wang, Y., Xu, W., Liu, Y., and Ding, Y. (2016). The strong El Nino of 2015/16 and its dominant impacts on global and China’s climate. Journal of Meteorological Research 30, 283–297.
The strong El Nino of 2015/16 and its dominant impacts on global and China’s climate.Crossref | GoogleScholarGoogle Scholar |