Phenotypic biomarkers of climatic impacts on declining insect populations: A key role for decadal drought, thermal buffering and amplification effects and host plant dynamics

Carnicer J., Stefanescu C., Vives-Ingla M., López C., Cortizas S., Wheat C., Vila R., Llusià J., Peñuelas J. (2019) Phenotypic biomarkers of climatic impacts on declining insect populations: A key role for decadal drought, thermal buffering and amplification effects and host plant dynamics. Journal of Animal Ecology. : 0-0.
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Doi: 10.1111/1365-2656.12933

Resum:

Widespread population declines have been reported for diverse Mediterranean butterflies over the last three decades, and have been significantly associated with increased global change impacts. The specific landscape and climatic drivers of these declines remain uncertain for most declining species. Here, we analyse whether plastic phenotypic traits of a model butterfly species (Pieris napi) perform as reliable biomarkers of vulnerability to extreme temperature impacts in natural populations, showing contrasting trends in thermally exposed and thermally buffered populations. We also examine whether improved descriptions of thermal exposure of insect populations can be achieved by combining multiple information sources (i.e., integrating measurements of habitat thermal buffering, habitat thermal amplification, host plant transpiration, and experimental assessments of thermal death time (TDT), thermal avoidance behaviour (TAB) and thermally induced trait plasticity). These integrative analyses are conducted in two demographically declining and two non-declining populations of P. napi. The results show that plastic phenotypic traits (butterfly body mass and wing size) are reliable biomarkers of population vulnerability to extreme thermal conditions. Butterfly wing size is strongly reduced only in thermally exposed populations during summer drought periods. Laboratory rearing of these populations documented reduced wing size due to significant negative effects of increased temperatures affecting larval growth. We conclude that these thermal biomarkers are indicative of the population vulnerability to increasing global warming impacts, showing contrasting trends in thermally exposed and buffered populations. Thermal effects in host plant microsites significantly differ between populations, with stressful thermal conditions only effectively ameliorated in mid-elevation populations. In lowland populations, we observe a sixfold reduction in vegetation thermal buffering effects, and larval growth occurs in these populations at significantly higher temperatures. Lowland populations show reduced host plant quality (C/N ratio), reduced leaf transpiration rates and complete above-ground plant senescence during the peak of summer drought. Amplified host plant temperatures are observed in open microsites, reaching thermal thresholds that can affect larval survival. Overall, our results suggest that butterfly population vulnerability to long-term drought periods is associated with multiple co-occurring and interrelated ecological factors, including limited vegetation thermal buffering effects at lowland sites, significant drought impacts on host plant transpiration and amplified leaf surface temperature, as well as reduced leaf quality linked to the seasonal advance of plant phenology. Our results also identify multiannual summer droughts affecting larval growing periods as a key driver of the recently reported butterfly population declines in the Mediterranean biome. © 2018 The Authors. Journal of Animal Ecology © 2018 British Ecological Society

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Contrasting impacts of precipitation on Mediterranean birds and butterflies

Herrando S., Titeux N., Brotons L., Anton M., Ubach A., Villero D., García-Barros E., Munguira M.L., Godinho C., Stefanescu C. (2019) Contrasting impacts of precipitation on Mediterranean birds and butterflies. Scientific Reports. 9: 0-0.
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Doi: 10.1038/s41598-019-42171-4

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The climatic preferences of the species determine to a large extent their response to climate change. Temperature preferences have been shown to play a key role in driving trends in animal populations. However, the relative importance of temperature and precipitation preferences is still poorly understood, particularly in systems where ecological processes are strongly constrained by the amount and timing of rainfall. In this study, we estimated the role played by temperature and precipitation preferences in determining population trends for birds and butterflies in a Mediterranean area. Trends were derived from long-term biodiversity monitoring data and temperature and precipitation preferences were estimated from species distribution data at three different geographical scales. We show that population trends were first and foremost related to precipitation preferences both in birds and in butterflies. Temperature preferences had a weaker effect on population trends, and were significant only in birds. The effect of precipitation on population trends operated in opposite directions in the two groups of species: butterfly species from arid environments and bird species from humid habitats are decreasing most. Our results indicate that, although commonly neglected, water availability is likely an important driver of animal population change in the Mediterranean region, with highly contrasting impacts among taxonomical groups. © 2019, The Author(s).

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Monitoring environmental effects on farmland Lepidoptera: Does necessary sampling effort vary between different bio-geographic regions in Europe?

Lang A., Kallhardt F., Lee M.S., Loos J., Molander M.A., Muntean I., Pettersson L.B., Rákosy L., Stefanescu C., Messéan A. (2019) Monitoring environmental effects on farmland Lepidoptera: Does necessary sampling effort vary between different bio-geographic regions in Europe?. Ecological Indicators. 102: 791-800.
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Doi: 10.1016/j.ecolind.2019.03.035

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In agro-ecosystems, environmental monitoring is fundamental to detect and survey changes related to land use change and management practices. Butterflies and moths have often been suggested as suitable indicators for monitoring environmental effects on biodiversity in farmlands. Here, we estimated the required sample size and monitoring effort necessary to run a Lepidoptera survey in European farmland, assessing in particular if monitoring investment would differ between representative bio-geographical regions. We operated linear 1-km long transect routes in farmland of Romania, Spain and Sweden from 2013 to 2015, and recorded butterflies and burnet moths (Papilionoidea, Zygaenidae). The transects were walked back and forth four times a season, and replicated yearly. The lepidopteran diversity was high in farmlands of Romania and Spain, but comparatively low in Sweden. The coefficient of variation (CV) of recorded species number differed between countries being lowest in Sweden and highest in Spain. In general, the CV dropped above a transect length of 400–800 m, thus indicating an increase in statistical power. Assuming a non-parametric test for matched samples, power calculations were conducted with the raw count data and with log-transformed count data for comparison. When using log-transformed data, the required sample size to detect an effect was less than 10 transects per country or region (in order to detect a 10% loss of species or a decrease of 30% in total abundance). Specific subgroups of species, e.g. protected species or specific indicator groups, showed a higher variance, thus requiring a higher sample size to detect effects ranging from 12 to 16 transects (equivalent to 21–29 working days per country and year). When using original, untransformed count data a considerably larger sample size would be needed. Actual time to be invested in field work differed between countries due to contrasting regional constraints and conditions. Nevertheless, the final monitoring effort in working days was similar between countries as the factors involved balanced out each other, in particular due to the differing year-to-year variations. Our study demonstrated the feasibility of an environmental monitoring programme in arable land using farmland butterflies across Europe. We present a suitable approach and guidelines as well as the necessary effort to be invested in future Europe-wide monitoring programmes of butterflies in agro-ecosystems, based on predictions of statistical power. © 2019

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Adaptive responses of animals to climate change are most likely insufficient

Radchuk V., Reed T., Teplitsky C., van de Pol M., Charmantier A., Hassall C., Adamík P., Adriaensen F., Ahola M.P., Arcese P., Miguel Avilés J., Balbontin J., Berg K.S., Borras A., Burthe S., Clobert J., Dehnhard N., de Lope F., Dhondt A.A., Dingemanse N.J., Doi H., Eeva T., Fickel J., Filella I., Fossøy F., Goodenough A.E., Hall S.J.G., Hansson B., Harris M., Hasselquist D., Hickler T., Joshi J., Kharouba H., Martínez J.G., Mihoub J.-B., Mills J.A., Molina-Morales M., Moksnes A., Ozgul A., Parejo D., Pilard P., Poisbleau M., Rousset F., Rödel M.-O., Scott D., Senar J.C., Stefanescu C., Stokke B.G., Kusano T., Tarka M., Tarwater C.E., Thonicke K., Thorley J., Wilting A., Tryjanowski P., Merilä J., Sheldon B.C., Pape Møller A., Matthysen E., Janzen F., Dobson F.S., Visser M.E., Beissinger S.R., Courtiol A., Kramer-Schadt S. (2019) Adaptive responses of animals to climate change are most likely insufficient. Nature Communications. 10: 0-0.
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Doi: 10.1038/s41467-019-10924-4

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Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species. © 2019, The Author(s).

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