Abstract
Increases in temperature have been predicted and reported for the Mediterranean mountain ranges due to global warming and this phenomenon is expected to have profound consequences on biodiversity and ecosystem functioning. We hereby present the case of Gentiana lutea L. subsp. lutea, a rhizomatous long-lived plant living in Central-Southern Europe, which is at the edge of its ecological and distributional range in Sardinia. Concretely, we analysed the reproductive success experienced during three phenological cycles (2013/2014, 2014/2015 and 2015/2016) in four representative populations, with particular attention to the phenological cycle of 2014/2015, which has been recorded as one of the warmest periods of the last decades. The Smirnov-Grubbs test was used to evaluate differences in temperature and precipitation regimes among historical data and the analysed years, while the Kruskal-Wallis followed by the Wilcoxon test was used to measure differences between anthesis and reproductive performances among cycles and populations. In addition, generalised linear models were carried out to check relationships between climate variables and reproductive performance. Significant differences among climate variables and analysed cycles were highlighted, especially for maximum and mean temperatures. Such variations determined a non-flowering stage in two of the four analysed populations in 2014/2015 and significant differences of further five reproductive traits among cycles. These results confirmed that in current unstable climatic conditions, which are particularly evident in seasonal climates, reproductive success can be a sensitive and easily observable indicator of climatic anomalies. Considering the importance of this issue and the ease and cost-effectiveness of reproductive success monitoring, we argue that research in this sense can be a supporting tool for the enhancement of future crucial targets such as biodiversity conservation and the mitigation of global warming effects.
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References
Abeli T, Rossi G, Gentili R, Gandini M, Mondoni A, Cristofanelli P (2012a) Effect of the extreme summer heat waves on isolated populations of two orophitic plants in the north Apennines (Italy). Nord J Bot 30:109–115. https://doi.org/10.1111/j.1756-1051.2011.01303.x
Abeli T, Rossi G, Gentili R, Mondoni A, Cristofanelli P (2012b) Response of alpine plant flower production to temperature and snow cover fluctuation at the species range boundary. Plant Ecol 213:1–13. https://doi.org/10.1007/s11258-011-0001-5
Abeli T, Gentili R, Mondoni A, Orsenigo S, Rossi G (2014) Effects of marginality on plant population performance. J Biogeogr 41:239–249. https://doi.org/10.1111/jbi.12215
Arft AM, Walker MD, Gurevitch J, Alatalo JM, Bret-Harte MS, Dale M, Diemer M, Gugerli F, Henry GHR, Jones MH, Hollister R, Jónsdóttir IS, Laine K, Lévesque E, Marion GM, Molau U, Mølgaard P, Nordenhäll U, Raszhivin V, Robinson CH, Starr G, Stenström A, Stenström M, Totland Ø, Turner L, Walker L, Webber P, Welker JM, Wookey PA (1999) Response patterns of tundra plant species to experimental warming: a meta-analysis of the international tundra experiment. Ecol Monogr 69:491–511. https://doi.org/10.1890/0012-9615(1999)069[0491:ROTPTE]2.0.CO
Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421. https://doi.org/10.1890/03-8024
Bacchetta G, Fenu G, Guarino R, Mandis G, Mattana E, Nieddu G, Scudu C (2013) Floristic traits and biogeographic characterization of the Gennargentu massif (Sardinia). Candollea 68:209–220. https://doi.org/10.15553/c2012v682a4
Barbosa AM, Brown JA, Real R (2017) modEvA: model evaluation and analysis. R package, version 1.3.3. https://cran.r-project.org/web/packages/modEvA/index.html. Accessed 11 Jan 2017
Caffarra A, Donnelly A (2011) The ecological significance of phenology in four different tree species: effects of light and temperature on bud burst. Int J Biometeorol 55:711–721. https://doi.org/10.1007/s00484-010-0386-1
Calvo R (1990) Four-year growth and reproduction of Cyclopogon cranichoides (Orchidaceae) in South Florida. Am J Bot 77:736–741. https://doi.org/10.2307/2444365
Carbognani M, Bernareggi G, Perucco F, Tomaselli M, Petraglia A (2016) Micro-climatic controls and warming effects on flowering time in alpine snowbeds. Oecologica 182:573–586. https://doi.org/10.1007/s00442-016-3669-3
Ciais P, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noble AD, Friend N, Friedlingstein P, Grünwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentini R (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533. https://doi.org/10.1038/nature03972
Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365. https://doi.org/10.1016/j.tree.2007.04.003
Cook BI, Wolkovich EM, Parmesan C (2012) Divergent responses to spring and winter warming drive community level flowering trends. Proc Natl Acad Sci 109:9000–9005. https://doi.org/10.1073/pnas.1118364109
Cuena-Lombraña A, Porceddu M, Dettori CA, Bacchetta G (2016) Gentiana lutea L. subsp. lutea seed germination: natural versus controlled conditions. Botany 94:653–659. https://doi.org/10.1139/cjb-2016-0030
De Frenne P, Graae BJ, Kolb A, Brunet J, Chabrerie O, Cousins SA et al (2010) Significant effects of temperature on the reproductive output of the forest herb Anemone nemorosa L. For Ecol Manag 259:809–817. https://doi.org/10.1016/j.foreco.2009.04.038
Diaz S, Cabido M (1997) Plant functional types and ecosystem function in relation to global change. J Veg Sci 8:463–474. https://doi.org/10.2307/3237198
Dormann CF, Woodin SJ (2002) Climate change in the Arctic: using plant functional types in a meta-analysis of field experiments. Funct Ecol 16:4–17. https://doi.org/10.1046/j.0269-8463.2001.00596.x
Fenu G, Mattana E, Bacchetta G (2011) Distribution, status and conservation of a critically endangered, extremely narrow endemic: Lamyropsis microcephala (Asteraceae) in Sardinia. Oryx 45:180–186. https://doi.org/10.1017/S0030605310001122
Fois M, Fenu G, Cuena-Lombraña A, Cogoni D, Bacchetta G (2015) A practical method to speed up the discovery of unknown populations using species distribution models. J Nat Conserv 24:42–48. https://doi.org/10.1016/j.jnc.2015.02.001
Fois M, Cuena-Lombraña A, Fenu G, Cogoni D, Bacchetta G (2016) The reliability of conservation status assessments at regional level: past, present and future perspectives on Gentiana lutea L. ssp. lutea in Sardinia. J Nat Conserv 33:1–9. https://doi.org/10.1016/j.jnc.2016.06.001
Fois M, Cuena-Lombraña A, Fenu G, Cogoni D, Bacchetta G (2018) Does a correlation exist between environmental suitability models and plant population parameters? An experimental approach to measure the influence of disturbances and environmental changes. Ecol Indic 86:1–8. https://doi.org/10.1016/j.ecolind.2017.12.009
Galen C, Stanton ML (1993) Short-term responses of alpine buttercups to experimental manipulations of growing season length. Ecology 74:1052–1058. https://doi.org/10.2307/1940475
Gentili R, Armiraglio S, Sgorbati S, Baroni C (2013) Geomorphological disturbance affects ecological driving forces and plant turnover along an altitudinal stress gradient on alpine slopes. Plant Ecol 214:571–586. https://doi.org/10.1007/s11258-013-0190-1
Giménez-Benavides L, Escudero A, Iriondo JM (2007) Reproductive limits of a late flowering high-mountain Mediterranean plant along an elevational climate gradient. New Phytol 173:367–382. https://doi.org/10.1111/j.1469-8137.2006.01932.x
Giménez-Benavides L, Escudero A, García-Camacho R, García-Fernández A, Iriondo JM, Lara-Romero C, Morente-López J (2018) How does climate change affect regeneration of Mediterranean high-mountain plants? An integration and synthesis of current knowledge. Plant Biol 20:50–62. https://doi.org/10.1111/plb.12643
Gordo O, Sanz JJ (2010) Impact of climate change on plant phenology in Mediterranean ecosystems. Glob Chang Biol 16:1082–1106. https://doi.org/10.1111/j.1365-2486.2009.02084.x
Grabherr G, Gottfried M, Pauli H (2010) Climate change impacts in alpine environments. Geogr Compass 4:1133–1153. https://doi.org/10.1111/j.1749-8198.2010.00356.x
Grubbs FE (1950) Sample criteria for testing outlying observations. Ann Math Stat 21:27–58. https://doi.org/10.1214/aoms/1177729885
Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecol Model 135:147–186. https://doi.org/10.1016/S0304-3800(00)00354-9
Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467. https://doi.org/10.1111/j.1461-0248.2005.00739.x
Hannah L, Lovejoy TE, Schneider SH (2005) Biodiversity and climate change in context. In: Lovejoy TE, Hannah L (eds) Climate change and biodiversity. Yale University Press, New Haven, pp 3–14
Hedhly A (2011) Sensitivity of flowering plant gametophytes to temperature fluctuations. Environ Exp Bot 74:9–16. https://doi.org/10.1016/j.envexpbot.2011.03.016
Hegi G (1966) Illustrierte Flora Von Mitteleuropa, Band 5, Teil 3. JF Lehmenns-Verlag, München
Hesse E, Rees M, Müller-Schärer H (2007) Seed bank persistence of clonal weeds in contrasting habitats: implications for control. Plant Ecol 190:233–243. https://doi.org/10.1007/s11258-006-9203-7
Hoffman AA, Parsons PA (1997) Extreme environmental change and evolution. Cambridge University Press, Cambridge
Holway JG, Ward RT (1965) Phenology of alpine plants in northern Colorado. Ecology 46:73–83. https://doi.org/10.2307/1935259
Hovenden MJ, Wills KE, Chaplin RE, Vander Schoor JK, Williams AL, Osanai YUI, Newton PC (2008) Warming and elevated CO2 affect the relationship between seed mass, germinability and seedling growth in Austrodanthonia caespitose, a dominant Australian grass. Glob Chang Biol 14:1633–1641. https://doi.org/10.1111/j.1365-2486.2008.01597.x
Huelber K, Gottfried M, Pauli H, Reiter K, Winkler M, Grabherr G (2006) Phenological responses of snowbed species to snow removal dates in the Central Alps: implications for climate warming. Arct Antarct Alp Res 38:99–103. https://doi.org/10.1657/1523-0430(2006)038[0099:PROSST]2.0.CO;2
Iler AM, Inouye DW, Høye TT, Miller-Rushing AJ, Burkle LA, Johnston EB (2013) Maintenance of temporal synchrony between syrphid flies and floral resources despite differential phenological responses to climate. Glob Chang Biol 19:2348–2359. https://doi.org/10.1111/gcb.12246
Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362. https://doi.org/10.1890/06-2128.1
Jacques MH, Lapointe L, Rice K, Montgomery RA, Stefanski A, Reich PB (2015) Responses of two understory herbs, Maianthemum canadense and Eurybia macrophylla, to experimental forest warming: early emergence is the key to enhanced reproductive output. Am J Bot 102:1610–1624. https://doi.org/10.3732/ajb.1500046
Kawai Y, Kudo G (2011) Local differentiation of flowering phenology in an alpine snowbed herb Gentiana nipponica. Botany 89:361–367. https://doi.org/10.1139/B11-024
Kery M, Matthies D, Spillmann HH (2000) Reduced fecundity and offspring performance in small populations of the declining grassland plants Primula veris and Gentiana lutea. J Ecol 88:17–30. https://doi.org/10.1046/j.1365-2745.2000.00422.x
Khanduri VP, Sharma CM, Singh SP (2008) The effects of climate change on plant phenology. Environmentalist 28:143–147. https://doi.org/10.1007/s10669-007-9153-1
Komsta L (2011) Outliers: tests for outliers. R package version 0.14. http://www.r-project.org, http://www.komsta.net. Accessed 10 Sept 2017
Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems; with 47 tables. Springer Science & Business Media, Heidelberg
Körner C, Hiltbrunner E (2018) The 90 ways to describe plant temperature. Perspect Plant Ecol 30:16–21. https://doi.org/10.1016/j.ppees.2017.04.004
Kramer K, Leinonen I, Loustau D (2000) The importance of phenology for the evaluation of impact of climate change on growth of boreal, temperate and Mediterranean forests ecosystems: an overview. Int J Biometeorol 44:67–75. https://doi.org/10.1007/s004840000066
Ladinig U, Pramsohler M, Bauer I, Zimmermann S, Neuner G, Wagner J (2015) Is sexual reproduction of high-mountain plants endangered by heat? Oecologia 177:1195–1210. https://doi.org/10.1007/s00442-015-3247-0
Luoto M, Heikkinen RK, Pöyry J, Saarinen K (2006) Determinants of the biogeographical distribution of butterflies in boreal regions. J Biogeogr 33:1764–1778. https://doi.org/10.1111/j.1365-2699.2005.01395.x
Luzuriaga AL, Escudero A, Albert MJ, Giménez-Benavides L (2006) Population structure effect on reproduction of a rare plant: beyond population size effect. Botany 84:1371–1379. https://doi.org/10.1139/b06-078
Mattana E, Fenu G, Bacchetta G (2012) Seed production and in situ germination of Lamyropsis microcephala (Asteraceae), a threatened Mediterranean mountain species. Arct Antarct Alp Res 44:343–349. https://doi.org/10.1657/1938-4246-44.3.343
NOAA (2017) National centers for environmental information. State of the climate: global analysis for annual 2016. Published online January 2017. Retrieved on Jan 19. 2017 from http://www.ncdc.noaa.gov/sotc/global/201613
Orsenigo S, Mondoni A, Rossi G, Abeli T (2014) Some like it hot and some like it cold, but not too much: plant responses to climate extremes. Plant Ecol 215:677–688. https://doi.org/10.1007/s11258-014-0363-6
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. https://doi.org/10.1038/nature01286
Parmesan C, Root TL, Willig MR (2000) Impacts of extreme weather and climate on terrestrial biota. Bull Am Meteor Soc 81:443–450. https://doi.org/10.1175/1520-0477(2000)081<0443:IOEWAC>2.3.CO
Pellissier L, Bråthen KA, Vittoz P, Yoccoz NG, Dubuis A, Meier ES, Zimmermann NE, Randin CF, Thuiller W, Garraud L, Van Es J, Guisan A (2013) Thermal niches are more conserved at cold than warm limits in arctic-alpine plant species. Glob Ecol Biogeogr 22:933–941. https://doi.org/10.1111/geb.12057
Peñuelas J, Boada M (2003) A global change-induced biome shift in the Montseny mountains (NE Spain). Glob Chang Biol 9:131–140. https://doi.org/10.1046/j.1365-2486.2003.00566.x
Preston JC, Sandve SR (2013) Adaptation to seasonality and the winter freeze. Front Plant Sci 4:167. https://doi.org/10.3389/fpls.2013.00167
R Development Core Team (2015) R: a language and environment for statistical computing. 3.2.2. R Foundation for Statistical Computing, Vienna
Rehm EM, Olivas P, Stroud J, Feeley KJ (2015) Losing your edge: climate change and the conservation value of range-edge populations. Ecol Evol 5:4315–4326. https://doi.org/10.1002/ece3.1645
Ren W, Hu N, Hou X, Zhang J, Guo H, Liu Z, Kong L, Wu Z, Wang H, Li X (2017) Long-term overgrazing-induced memory decreases photosynthesis of clonal offspring in a perennial grassland plant. Front Plant Sci 8:419. https://doi.org/10.3389/fpls.2017.00419
Rossi M, Fisogni A, Nepi M, Quaranta M, Galloni M (2014) Bouncy versus idles: on the different role of pollinators in the generalist Gentiana lutea L. Flora 209:164–171. https://doi.org/10.1016/j.flora.2014.02.002
Rossi M, Fisogni A, Galloni M (2016) Biosystematic studies on the mountain plant Gentiana lutea L. reveal variability in reproductive traits among subspecies. Plant Ecol Divers 9:97–104. https://doi.org/10.1080/17550874.2015.1074625
Scherrer D, Körner C (2011) Topographically controlled thermal-habitat differentiation buffers alpine plant diversity against climate warming. J Biogeogr 38:406–416. https://doi.org/10.1111/j.1365-2699.2010.02407.x
Schwartz MD, Hanes JM (2010) Continental-scale phenology: warming and chilling. Int J Climatol 30:1595–1598. https://doi.org/10.1002/joc.2014
Sih A, Baltus MS (1987) Patch size, pollinator behavior, and pollinator limitation in catnip. Ecology 68:1679–1690. https://doi.org/10.2307/1939860
Struwe L, Albert VA (2002) Gentianaceae: systematics and natural history. Cambridge University Press, Cambridge
Walker X, Henry GH, McLeod K, Hofgaard A (2012) Reproduction and seedling establishment of Picea glauca across the northernmost forest-tundra region in Canada. Glob Chang Biol 18:3202–3211. https://doi.org/10.1111/j.1365-2486.2012.02769.x
Walsh C, Mac Nally R (2008) Hier.Part: hierarchical partitioning. R Package. Retrieved on July 15, 2015 from: http://cran.r-project.org/web/packages/hier.part/index.html
Watkinson AR, Newsham KK, Forrester L (1998) Vulpia ciliata Dumort. ssp. ambigua (Le Gall) Stace & Auquier (Vulpia ambigua (Le Gall) More, Festuca ambigua Le Gall). J Ecol 86:690–705. https://doi.org/10.1046/j.1365-2745.1998.00296.x
WMO-World Meteorological Organization, Scientific Assessment of Ozone Depletion (2003) Global ozone research and monitoring project-report no. 47. World Meteorological Organization, Geneva
Woodward FI, Williams BG (1987) Climate and plant distribution at global and local scales. Plant Ecol 69:189–197
Acknowledgements
The authors thank the FoReSTAS Agency for the logistic support. We are grateful to Martin Barry for reading the manuscript and giving linguistic advice. We also thank the anonymous reviewers for their constructive and valuable comments on the manuscript.
Funding
This research was supported by the ‘Progetto pilota per la conservazione in situ ed ex situ, caratterizzazione genetica, rinforzo popolazionale e reintroduzione di Gentiana lutea L.’ (Regione Autonoma della Sardegna, Rep. 27512-91 del 9-XII-2013 RAS).
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Cuena-Lombraña, A., Fois, M., Fenu, G. et al. The impact of climatic variations on the reproductive success of Gentiana lutea L. in a Mediterranean mountain area. Int J Biometeorol 62, 1283–1295 (2018). https://doi.org/10.1007/s00484-018-1533-3
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DOI: https://doi.org/10.1007/s00484-018-1533-3