The ghost of past climate acting on present-day plant diversity: Lessons from a climate-based delimitation of the tropical alpine ecosystem

Martha Kandziora1(), Juan M. Gorospe1,2, Luciana Salomon1, Diana L. A. Vásquez2, Maria Pinilla Vargas1, Filip Kolář1,2, Petr Sklenář1, Roswitha Schmickl1,2

PDF
Journal of Systematics and Evolution ›› 2024, Vol. 62 ›› Issue (2) : 275-290. DOI: 10.1111/jse.13048
Research Article

The ghost of past climate acting on present-day plant diversity: Lessons from a climate-based delimitation of the tropical alpine ecosystem

  • Martha Kandziora1(), Juan M. Gorospe1,2, Luciana Salomon1, Diana L. A. Vásquez2, Maria Pinilla Vargas1, Filip Kolář1,2, Petr Sklenář1, Roswitha Schmickl1,2
Author information +
History +

Abstract

Habitat stability is important for maintaining biodiversity by preventing species extinction, but this stability is being challenged by climate change. The tropical alpine ecosystem is currently one of the ecosystems most threatened by global warming, and the flora close to the permanent snow line is at high risk of extinction. The tropical alpine ecosystem, found in South and Central America, Malesia and Papuasia, Africa, and Hawaii, is of relatively young evolutionary age, and it has been exposed to changing climates since its origin, particularly during the Pleistocene. Estimating habitat loss and gain between the Last Glacial Maximum (LGM) and the present allows us to relate current biodiversity to past changes in climate and habitat stability. In order to do so, (i) we developed a unifying climate-based delimitation of tropical alpine regions across continents, and (ii) we used this delimitation to assess the degree of habitat stability, that is, the overlap of suitable areas between the LGM and the present, in different tropical alpine regions. Finally, we discuss the link between habitat stability and tropical alpine plant diversity. Our climate-based delimitation approach can be easily applied to other ecosystems using our developed code, facilitating macro-comparative studies of habitat dynamics through time.

Keywords

extinction risk / habitat dynamics / Last Glacial Maximum / plant diversity / refugia / tropical alpine

Cite this article

Download citation ▾
Martha Kandziora, Juan M. Gorospe, Luciana Salomon, Diana L. A. Vásquez, Maria Pinilla Vargas, Filip Kolář, Petr Sklenář, Roswitha Schmickl. The ghost of past climate acting on present-day plant diversity: Lessons from a climate-based delimitation of the tropical alpine ecosystem. Journal of Systematics and Evolution, 2024, 62(2): 275‒290 https://doi.org/10.1111/jse.13048

References

1 JRM Allen, T Hickler, JS Singarayer, MT Sykes, PJ Valdes, B Huntley. 2010. Last glacial vegetation of northern Eurasia. Quaternary Science Reviews 29: 2604–2618.
2 A Antonelli. 2009. Have giant lobelias evolved several times independently? Life form shifts and historical biogeography of the cosmopolitan and highly diverse subfamily Lobelioideae (Campanulaceae). BMC Biology 7: 82.
3 MTK Arroyo, L Dudley, P Pliscoff, LA Cavieres, FA Squeo, C Marticorena, R Rozzi. 2010. A possible correlation between the altitudinal and latitudinal ranges of species in the high elevation flora of the Andes. In: Spehn EM, Körner C eds. Data Mining for Global Trends in Mountain Biodiversity. Boca Raton, Florida, USA: CRC Press Taylor and Francis. 39–47.
4 MTK Arroyo, LA Cavieres. 2013. High-elevation Andean ecosystems. In: Levin SA ed. Encyclopedia of biodiversity. 2nd ed. Waltham: Academic Press. 96–110.
5 TL Ashman, TM Knight, JA Steets, P Amarasekare, M Burd, DR Campbell, MR Dudash, MO Johnston, SJ Mazer, RJ Mitchell, MT Morgan, WG Wilson. 2004. Pollen limitation of plant reproduction: Ecological and evolutionary causes and consequences. Ecology 85: 2408–2421.
6 MY Bader, M Rietkerk, AK Bregt. 2007. Vegetation structure and temperature regimes of tropical alpine treelines. Arctic, Antarctic, and Alpine Research 39: 353–364.
7 PJ Bartlein, SP Harrison, S Brewer, S Connor, BAS Davis, K Gajewski, J Guiot, TI Harrison-Prentice, A Henderson, O Peyron, IC Prentice, M Scholze, H Seppä, B Shuman, S Sugita, RS Thompson, AE Viau, J Williams, H Wu. 2011. Pollen-based continental climate reconstructions at 6 and 21 ka: A global synthesis. Climate Dynamics 37: 775–802.
8 L Berio Fortini, PD Krushelnycky, DR Drake, F Starr, K Starr, CG Chimera. 2022. Complex demographic responses to contrasting climate drivers lead to divergent population trends across the range of a threatened alpine plant. Global Ecology and Conservation 33: e01954.
9 RS Bivand, E Pebesma, V Gomez-Rubio. 2013. Applied spatial data analysis with R. 2nd ed. New York, NY: Springer.
10 C Blanco-Gavaldà, M Galbany-Casals, A Susanna, S Andrés-Sánchez, RJ Bayer, C Brochmann, GV Cron, NG Bergh, N Garcia-Jacas, A Gizaw, M Kandziora, F Kolář, J López-Alvarado, F Leliaert, R Letsara, LD Moreyra, SG Razafimandimbison, R Schmickl, C Roquet. 2023. Repeatedly northwards and upwards: Southern African grasslands fuel the colonization of the African sky islands in Helichrysum (Compositae). Plants 12: 2213.
11 C Brochmann, A Gizaw, D Chala, M Kandziora, G Eilu, M Popp, MD Pirie, B Gehrke. 2021. History and evolution of the afroalpine flora: In the footsteps of Olov Hedberg. Alpine Botany 132: 65–87.
12 W Buytaert, F Cuesta-Camacho, C Tobón. 2011. Potential impacts of climate change on the environmental services of humid tropical alpine regions. Global Ecology and Biogeography 20: 19–33.
13 P Carnicero, J Wessely, D Moser, X Font, S Dullinger, P Schönswetter. 2022. Postglacial range expansion of high-elevation plants is restricted by dispersal ability and habitat specialization. Journal of Biogeography 49: 1739–1752.
14 D Chala, C Brochmann, A Psomas, D Ehrich, A Gizaw, CA Masao, V Bakkestuen, NE Zimmermann. 2016. Good-bye to tropical alpine plant giants under warmer climates? Loss of range and genetic diversity in Lobelia rhynchopetalum. Ecology and Evolution 6: 8931–8941.
15 D Chala, NE Zimmermann, C Brochmann, V Bakkestuen. 2017. Migration corridors for alpine plants among the ‘sky islands’ of eastern Africa: Do they, or did they exist? Alpine Botany 127: 133–144.
16 PU Clark, AS Dyke, JD Shakun, AE Carlson, J Clark, B Wohlfarth, JX Mitrovica, SW Hostetler, AM McCabe. 2009. The last glacial maximum. Science 325: 710–714.
17 N Contreras-Ortiz, GW Atchison, CE Hughes, S Madriňán. 2018. Convergent evolution of high elevation plant growth forms and geographically structured variation in Andean Lupinus (Fabaceae). Botanical Journal of the Linnean Society 187: 118–136.
18 F Cuesta, C Tovar, LD Llambí, WD Gosling, S Halloy, J Carilla, P Muriel, RI Meneses, S Beck, C Ulloa Ulloa, K Yager, N Aguirre, P Viñas, J Jácome, D Suárez-Duque, W Buytaert, H Pauli. 2020. Thermal niche traits of high alpine plant species and communities across the tropical Andes and their vulnerability to global warming. Journal of Biogeography 47: 408–420.
19 R Daubenmire. 1954. Alpine timberlines in the Americas and their interpretation. Butler University Botanical Studies 11: 119–136.
20 A Dobson, Z Rowe, J Berger, P Wholey, T Caro. 2021. Biodiversity loss due to more than climate change. Science 374: 699–700.
21 E Dušková, P Sklenář, F Kolář, DLA Vásquez, K Romoleroux, T Fér, K Marhold. 2017. Growth form evolution and hybridization in Senecio (Asteraceae) from the high equatorial Andes. Ecology and Evolution 7: 6455–6468.
22 S Fei, JM Desprez, KM Potter, I Jo, JA Knott, CM Oswalt. 2017. Divergence of species responses to climate change. Science Advances 3: e1603055.
23 A Feurdean, I Tanţău. 2017. The evolution of vegetation from the last glacial maximum until the present. In: Radoane M, Vespremeanu-Stroe A eds. Landform dynamics and evolution in Romania. Cham: Springer International Publishing. 67–83.
24 SE Fick, RJ Hijmans. 2017. WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37: 4302–4315.
25 SGA Flantua, A O'Dea, RE Onstein, C Giraldo, H Hooghiemstra. 2019. The flickering connectivity system of the north Andean páramos. Journal of Biogeography 46: 1808–1825.
26 CM Galván-Cisneros, PM Villa, AJP Coelho, PV Campos, JAA Meira-Neto. 2023. Altitude as environmental filtering influencing phylogenetic diversity and species richness of plants in tropical mountains. Journal of Mountain Science 20: 285–298.
27 B Gehrke. 2018. Staying cool: Preadaptation to temperate climates required for colonising tropical alpine-like environments. PhytoKeys 96: 111–125.
28 B Gehrke, M Kandziora, MD Pirie. 2016. The evolution of dwarf shrubs in alpine environments: A case study of Alchemilla in Africa. Annals of Botany 117: 121–131.
29 B Gehrke, HP Linder. 2009. The scramble for Africa: Pan-temperate elements on the African high mountains. Proceedings of the Royal Society B: Biological Sciences 276: 2657–2665.
30 B Gehrke, HP Linder. 2014. Species richness, endemism and species composition in the tropical Afroalpine flora. Alpine Botany 124: 165–177.
31 O Hedberg. 1961. The phytogeographical position of the afroalpine flora. Recent Advances Botany 1: 914–919.
32 O Hedberg. 1964. Features of afroalpine plant ecology: avec un résumé en francais. Uppsala: Almqvist & Wiksell.
33 A Hemp. 2005. Climate change-driven forest fires marginalize the impact of ice cap wasting on Kilimanjaro. Global Change Biology 11: 1013–1023.
34 RJ Hijmans. 2023. raster: Geographic Data analysis and modeling. R package version 3.3.6.
35 JW Hollister. 2022. elevatr: Access elevation data from various APIs. R package version 0.4.4.
36 Holtmeier FK ed. 2009. Mountain timberlines. Netherlands: Springer.
37 H Hooghiemstra, T van der Hammen. 2004. Quaternary Ice-Age dynamics in the Colombian Andes: developing an understanding of our legacy. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 359: 173–181.
38 B. Huntley, MJ Alfano, JRM Allen, D Pollard, PC Tzedakis, J-L Beaulieu, E de Grüger, B. Watts 2003. European vegetation during Marine Oxygen Isotope Stage-3. Quaternary Research 59: 195–212.
39 IPCC. 2023. Climate Change 2023: Synthesis report. In: Core Writing Team, Lee H, Romero J eds. Contribution of working groups I, II and III to the sixth assessment report of the intergovernmental panel on climate change. Geneva, Switzerland: IPCC. 184.
40 RS Jabaily, KJ Sytsma. 2013. Historical biogeography and life-history evolution of Andean Puya (Bromeliaceae). Botanical Journal of the Linnean Society 171: 201–224.
41 V Janská, B Jiménez-Alfaro, M Chytrý, J Divíšek, O Anenkhonov, A Korolyuk, N Lashchinskyi, M Culek. 2017. Palaeodistribution modelling of European vegetation types at the Last Glacial Maximum using modern analogues from Siberia: Prospects and limitations. Quaternary Science Reviews 159: 103–115.
42 M Kandziora, B Gehrke, M Popp, A Gizaw, C Brochmann, MD Pirie. 2022a. The enigmatic tropical alpine flora on the African sky islands is young, disturbed, and unsaturated. Proceedings of the National Academy of Sciences of the United States of America 119: e2112737119.
43 M Kandziora, JW Kadereit, B Gehrke. 2016. Frequent colonization and little in situ speciation in Senecio in the tropical alpine-like islands of eastern Africa. American Journal of Botany 103: 1483–1498.
44 M Kandziora, P Sklenář, F Kolář, R Schmickl. 2022b. How to tackle phylogenetic discordance in recent and rapidly radiating groups? Developing a workflow using Loricaria (Asteraceae) as an example. Frontiers in Plant Science 12: 765719.
45 DN Karger, O Conrad, J Böhner, T Kawohl, H Kreft, RW Soria-Auza, NE Zimmermann, HP Linder, M Kessler. 2017. Climatologies at high resolution for the earth′s land surface areas. Scientific Data 4: 1–20.
46 DN Karger, M Kessler, O Conrad, P Weigelt, H Kreft, C König, NE Zimmermann. 2019. Why tree lines are lower on islands—Climatic and biogeographic effects hold the answer. Global Ecology and Biogeography 28: 839–850.
47 W Köppen. 1884. Die Wärmezonen der Erde, nach der Dauer der heissen, gemässigten und kalten Zeit und nach der Wirkung der Wärme auf die organische Welt betrachtet. Meteorologische Zeitschrift 1: 5–226.
48 C Körner. 2003. Alpine plant life: Functional plant ecology of high mountain ecosystems. Berlin: Springer.
49 C Körner, J Paulsen. 2004. A world–wide study of high altitude treeline temperatures. Journal of Biogeography 31: 713–732.
50 C Körner, J Paulsen, EM Spehn. 2011. A definition of mountains and their bioclimatic belts for global comparisons of biodiversity data. Alpine Botany 121: 73–78.
51 M Kottek, J Grieser, C Beck, B Rudolf, F Rubel. 2006. World map of the Köppen-Geiger climate classification updated. Meteorologische Zeitschrift 15: 259–263.
52 F Luebert, M Weigend. 2014. Phylogenetic insights into Andean plant diversification. Frontiers in Ecology and Evolution 2: 27.
53 J Luteyn. 1999. Introduction to the páramo ecosystem. In: Luteyn J ed. Paramos: A checklist of plant diversity, geographical distribution, and botanical literature. New York, NY: The New York Botanical Garden Press. 1–39.
54 S Madriñán, AJ Cortés, JE Richardson. 2013. Páramo is the world′s fastest evolving and coolest biodiversity hotspot. Frontiers in Genetics 4: 192.
55 J Maksic, IM Venancio, MH Shimizu, CM Chiessi, P Piacsek, G Sampaio, FW Cruz, FF Alexandre. 2022. Brazilian biomes distribution: Past and future. Palaeogeography, Palaeoclimatology, Palaeoecology 585: 110717.
56 L Mander, SW Punyasena. 2014. On the taxonomic resolution of pollen and spore records of earth′s vegetation. International Journal of Plant Sciences 175: 931–945.
57 S Manes, MJ Costello, H Beckett, A Debnath, E Devenish-Nelson, K-A Grey, R Jenkins, TM Khan, W Kiessling, C Krause, SS Maharaj, GF Midgley, J Price, G Talukdar, MM Vale. 2021. Endemism increases species′ climate change risk in areas of global biodiversity importance. Biological Conservation 257: 109070.
58 JM Mangen. 1993. Ecology and vegetation of Mt Trikora, New Guinea (Irian Jaya, Indonesia). Luxembourg: Musée national d′histoire naturelle de Luxembourg. 216
59 JE McCormack, H Huang, LL Knowles, R Gillespie, D Clague. 2009. Sky islands. Encyclopedia of Islands 4: 841–843.
60 C McWilliams, M Lurgi, JM Montoya, A Sauve, D Montoya. 2019. The stability of multitrophic communities under habitat loss. Nature Communications 10: 2322.
61 VS Merckx, KP Hendriks, KK Beentjes, CB Mennes, LE Becking, KT Peijnenburg, A Afendy, N Arumugam, H de Boer, A Biun, MM Buang, P-P Chen, AYC Chung, R Dow, FAA Feijen, H Feijen, C Feijen-van Soest, J Geml, R Geurts, B Gravendeel, P Hovenkamp, P Imbun, I Ipor, SB Janssens, M Jocqué, H Kappes, E Khoo, P Koomen, F Lens, RJ Majapun, LN Morgado, S Neupane, N Nieser, JT Pereira, H Rahman, S Sabran, A Sawang, RM Schwallier, P-S Shim, H Smit, N Sol, M Spait, M Stech, F Stokvis, JB Sugau, M Suleiman, S Sumail, DC Thomas, J van Tol, FYY Tuh, BE Yahya, J Nais, R Repin, M Lakim, M Schilthuizen. 2015. Evolution of endemism on a young tropical mountain. Nature 524: 347–350.
62 N Myers, RA Mittermeier, CG Mittermeier, GAB da Fonseca, J Kent. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853.
63 B Nevado, N Contreras-Ortiz, C Hughes, DA Filatov. 2018. Pleistocene glacial cycles drive isolation, gene flow and speciation in the high-elevation Andes. New Phytologist 219: 779–793.
64 NM Nürk, F Michling, HP Linder. 2018. Are the radiations of temperate lineages in tropical alpine ecosystems pre-adapted? Global Ecology and Biogeography 27: 334–345.
65 J Paulsen, C Körner. 2014. A climate-based model to predict potential treeline position around the globe. Alpine Botany 124: 1–12.
66 E Pebesma. 2018. Simple features for R: Standardized support for spatial vector data. The R Journal 10: 439–446.
67 E Pebesma, R Bivand. 2023. Spatial data science: With applications in R. London: Chapman and Hall/CRC. 352.
68 MC Peel, BL Finlayson, TA McMahon. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11: 1633–1644.
69 N Pepin, RS Bradley, HF Diaz, M Baraer, EB Caceres, N Forsythe, H Fowler, G Greenwood, MZ Hashmi, XD Liu, JR Miller, L Ning, A Ohmura, E Palazzi, I Rangwala, W Schöner, I Severskiy, M Shahgedanova, MB Wang, SN Williamson, DQ Yang, Mountain Research Initiative EDW Working Group. 2015. Elevation-dependent warming in mountain regions of the world. Nature Climate Change 5: 424–430.
70 G Peyre. 2022. What does the future hold for páramo plants? A modelling approach. Frontiers in Ecology and Evolution 10: 896387.
71 G Peyre, C Lopez, MD Diaz, J Lenoir. 2022. Climatic refugia in the coldest neotropical hotspot, the Andean páramo. bioRxiv.
72 G Peyre, D Osorio, R François, F Anthelme. 2021. Mapping the páramo land-cover in the Northern Andes. International Journal of Remote Sensing 42: 7777–7797.
73 SL Pimm. 2009. Climate disruption and biodiversity. Current Biology 19: R595–R601.
74 C Pouchon, A Fernández, JM Nassar, F Boyer, S Aubert, S Lavergne, J Mavárez. 2018. Phylogenomic analysis of the explosive adaptive radiation of the Espeletia complex (Asteraceae) in the tropical Andes. Systematic Biology 67: 1041–1060.
75 B Poulter, P Ciais, E Hodson, H Lischke, F Maignan, S Plummer, NE Zimmermann. 2011. Plant functional type mapping for earth system models. Geoscientific Model Development 4: 993–1010.
76 R Core Team. 2013. R: A Language and Environment for Statistical Computing. Vienna and Austria: R Foundation for Statistical Computing.
77 I Robiansyah. 2018. Assessing the impact of climate change on the distribution of endemic subalpine and alpine plants of New Guinea. Songklanakarin Journal of Science & Technology 40: 701–709.
78 P Royen. 1979. The alpine flora of New Guinea. Vaduz, Lichtenstein: J. Cramer - Pennsylvania State University.
79 B Saladin, L Pellissier, CH Graham, MP Nobis, N Salamin, NE Zimmermann. 2020. Rapid climate change results in long-lasting spatial homogenization of phylogenetic diversity. Nature Communications 11: 4663.
80 G Sarmiento. 1986. Ecological features of climate in high tropical mountains. High Altitude Tropical Biogeography 11: 45.
81 RJ Schley, AD Twyford, RT Pennington. 2022. Hybridization: A ‘double-edged sword’ for Neotropical plant diversity. Botanical Journal of the Linnean Society 199: 331–356.
82 P Sklenář, H Balslev. 2005. Superpáramo plant species diversity and phytogeography in Ecuador. Flora—Morphology, Distribution, Functional Ecology of Plants 200: 416–433.
83 P Sklenář, E Dušková, H Balslev. 2011. Tropical and temperate: Evolutionary history of páramo flora. The Botanical Review 77: 71–108.
84 P Sklenář, I Hedberg, AM Cleef. 2014. Island biogeography of tropical alpine floras. Journal of Biogeography 41: 287–297.
85 P Sklenář, R Jaramillo, SS Wojtasiak, RI Meneses, P Muriel, A Klimeš. 2023. Thermal tolerance of tropical and temperate alpine plants suggests that ‘mountain passes are not higher in the tropics. Global Ecology and Biogeography 32: 1073–1086.
86 RA Slatyer, M Hirst, JP Sexton. 2013. Niche breadth predicts geographical range size: A general ecological pattern. Ecology Letters 16: 1104–1114.
87 B Smith, IC Prentice, MT Sykes. 2001. Representation of vegetation dynamics in the modelling of terrestrial ecosystems: Comparing two contrasting approaches within European climate space. Global Ecology and Biogeography 10: 621–637.
88 A South. 2011. rworldmap: A new R package for mapping global data. The R Journal 3: 35–43.
89 M Steinthorsdottir, HK Coxall, AM Boer, M de Huber, N Barbolini, CD Bradshaw, NJ Burls, SJ Feakins, E Gasson, J Henderiks, AE Holbourn, S Kiel, MJ Kohn, G Knorr, WM Kürschner, CH Lear, D Liebrand, DJ Lunt, T Mörs, PN Pearson, MJ Pound, H Stoll, CaE Strömberg. 2021. The Miocene: The future of the past. Paleoceanography and Paleoclimatology 36: e2020PA004037.
90 AS Tarkan, L Vilizzi. 2015. Patterns, latitudinal clines and countergradient variation in the growth of roach Rutilus rutilus (Cyprinidae) in its Eurasian area of distribution. Reviews in Fish Biology and Fisheries 25: 587–602.
91 F Tererai, AR Wood. 2014. On the present and potential distribution of Ageratina adenophora (Asteraceae) in South Africa. South African Journal of Botany 95: 152–158.
92 R Testolin, F Attorre, P Borchardt, RF Brand, H Bruelheide, M Chytrý, M De Sanctis, J Dolezal, M Finckh, S Haider, A Hemp, U Jandt, M Kessler, AY Korolyuk, J Lenoir, N Makunina, GP Malanson, DB Montesinos-Tubée, J Noroozi, A Nowak, RK Peet, G Peyre, FM Sabatini, J Šibík, P Sklenář, SP Sylvester, K Vassilev, R Virtanen, W Willner, SK Wiser, EG Zibzeev, B Jiménez-Alfaro. 2021. Global patterns and drivers of alpine plant species richness. Global Ecology and Biogeography 30: 1218–1231.
93 JM Thornton, N Pepin, M Shahgedanova, C Adler. 2022. Coverage of in situ climatological observations in the world′s mountains. Frontiers in Climate 4: 814181.
94 C Tovar, CA Arnillas, F Cuesta, W Buytaert. 2013. Diverging responses of tropical Andean biomes under future climate conditions. PLOS ONE 8: e63634.
95 C Tovar, I Melcher, B Kusumoto, F Cuesta, A Cleef, RI Meneses, S Halloy, LD Llambí, S Beck, P Muriel, R Jaramillo, J Jácome, J Carilla. 2020. Plant dispersal strategies of high tropical alpine communities across the Andes. Journal of Ecology 108: 1910–1922.
96 C Tovar, AF Carril, AG Gutiérrez, A Ahrends, L Fita, P Zaninelli, P Flombaum, AM Abarzúa, D Alarcón, V Aschero, S Báez, A Barros, J Carilla, ME Ferrero, SGA Flantua, P Gonzáles, CG Menéndez, OA Pérez-Escobar, A Pauchard, RC Ruscica, T Särkinen, AA Sörensson, A Srur, R Villalba, PM Hollingsworth. 2022. Understanding climate change impacts on biome and plant distributions in the Andes: Challenges and opportunities. Journal of Biogeography 49: 1420–1442.
97 JB Valencia, J Mesa, JG León, S Madriñán, AJ Cortés. 2020. Climate vulnerability assessment of the Espeletia complex on Páramo sky islands in the northern Andes. Frontiers in Ecology and Evolution 8: 565708.
98 A Valiente-Banuet, MA Aizen, JM Alcántara, J Arroyo, A Cocucci, M Galetti, MB García, D García, JM Gómez, P Jordano, R Medel, L Navarro, JR Obeso, R Oviedo, N Ramírez, PJ Rey, A Traveset, M Verdú, R Zamora. 2015. Beyond species loss: The extinction of ecological interactions in a changing world. Functional Ecology 29: 299–307.
99 S Varela, MS Lima-Ribeiro, LC Terribile. 2015. A short guide to the climatic variables of the Last Glacial Maximum for biogeographers. PLOS ONE 10: e0129037.
100 OM Vargas, EM Ortiz, BB Simpson. 2017. Conflicting phylogenomic signals reveal a pattern of reticulate evolution in a recent high-Andean diversification (Asteraceae: Astereae: Diplostephium). New Phytologist 214: 1736–1750.
101 DLA Vásquez, MM Hansen, H Balslev, R Schmickl. 2022. Intraspecific genetic consequences of Pleistocene climate change on Lupinus microphyllus (Fabaceae) in the Andes. Alpine Botany 132: 273–284.
102 M Vuille, B Francou, P Wagnon, I Juen, G Kaser, BG Mark, RS Bradley. 2008. Climate change and tropical Andean glaciers: Past, present and future. Earth-Science Reviews 89: 79–96.
103 K Wesche, G Miehe, M Kaeppeli. 2000. The significance of fire for afroalpine ericaceous vegetation. Mountain Research and Development 20: 340–347.
104 F White. 1983. The vegetation of Africa, a descriptive memoir to accompany the UNESCO/AETFAT/UNSO vegetation map of Africa. Paris: UNESCO.
105 JW Williams, ST Jackson, JE Kutzbach. 2007. Projected distributions of novel and disappearing climates by 2100 AD. Proceedings of the National Academy of Sciences of the United States of America 104: 5738–5742.
106 A Zimmer, RI Meneses, A Rabatel, A Soruco, O Dangles, F Anthelme. 2018. Time lag between glacial retreat and upward migration alters tropical alpine communities. Perspectives in Plant Ecology, Evolution and Systematics 30: 89–102.
PDF

Accesses

Citations

Detail

Sections
Recommended

/