Skip to main content

Diversification in Ancient and Nutrient-Poor Neotropical Ecosystems: How Geological and Climatic Buffering Shaped Plant Diversity in Some of the World’s Neglected Hotspots

  • Chapter
  • First Online:

Part of the book series: Fascinating Life Sciences ((FLS))

Abstract

South America harbors the highest plant diversity on Earth. The causes of such exceptionally high diversity remain poorly understood, despite great attention devoted to the ecology and evolution of biota in productive and geologically recent ecosystems such as the Amazon forest and the Andes. Evidence suggests ancient and extremely nutrient-poor landscapes are major centers of plant diversity and endemism, and acted as interglacial refugia, but singularities of their evolutionary history have been overlooked. Here, we examine to what extent Ocbil theory (old, climatically-buffered, infertile landscapes) may prove useful in explaining diversification patterns in some of the most diverse Neotropical ecosystems. We propose a theoretical framework that encompasses a mechanistic explanation for the predictions of Ocbil theory, and links ecological and evolutionary processes to vegetation patterns and functional traits. We review diversification patterns and population genetics in campos rupestres vegetation in light of Ocbil theory. We propose areas of future research that will accelerate and improve our understanding on the ecology and evolution of Neotropical biota on ancient, nutrient-poor vegetation. This knowledge is expected to shed light on the complex history of Neotropical plant diversification and, ultimately, provide tools for their sustainable use and conservation.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Adeney JM, Christensen NL, Vicentini A, Cohn-Haft M (2016) White-sand ecosystems in Amazonia. Biotropica 48:7–23

    Google Scholar 

  • Alcântara S, Ree RH, Mello-Silva R (2018) Accelerated diversification and functional trait evolution in Velloziaceae reveal new insights into the origins of the campos rupestres’ exceptional floristic richness. Ann Bot 122:165–180

    PubMed  PubMed Central  Google Scholar 

  • Alves RVJ, Kolbek J (2010) Can campo rupestre vegetation be floristically delimited based on vascular plant genera? Plant Ecol 207:67–79

    Google Scholar 

  • Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA (2016) Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet 17:81–93

    CAS  PubMed  PubMed Central  Google Scholar 

  • Antonelli A, Sanmartín I (2011) Why are there so many plant species in the Neotropics? Taxon 60:403–414

    Google Scholar 

  • Antonelli A, Nylander JA, Persson C, Sanmartín I (2009) Tracing the impact of the Andean uplift on Neotropical plant evolution. Proc Natl Acad Sci USA 106:9749–9754

    CAS  PubMed  Google Scholar 

  • Antonelli A, Zizka A, Silvestro D, Scharn R, Cascales-Miñana B, Bacon CD (2015) An engine for global plant diversity: highest evolutionary turnover and emigration in the American tropics. Front Genet 6(130). https://doi.org/10.3389/fgene.2015.00130

  • Arditti J, Ghani AKA (2000) Numerical and physical properties of orchid seeds and their biological implications. New Phytol 145:367–421

    Google Scholar 

  • Armijo R, Lacassin R, Coudurier-Curveur A, Carrizo D (2015) Coupled tectonic evolution of Andean orogeny and global climate. Earth-Sci Rev 143:1–35

    Google Scholar 

  • Azevedo CO, Borba EL, van den Berg C (2006) Evidence of natural hybridization and introgression in Bulbophyllum involutum Borba, Semir & F. Barros and B. weddellii (Lindl.) Rchb. f. (Orchidaceae) in the Chapada Diamantina, Brazil, by using allozyme markers. Braz J Bot 29:415–421

    Google Scholar 

  • Azevedo MTA, Borba EL, Semir J, Solferini VN (2007) High genetic variability in Neotropical myophilous orchids. Bot J Linn Soc 153:33–40

    Google Scholar 

  • Barbará T, Lexer C, Martinelli G, Mayo S, Fay MF, Heuertz M (2008) Within-population spatial genetic structure in four naturally fragmented species of a neotropical inselberg radiation, Alcantarea imperialis, A. geniculata, A. glaziouana and A. regina (Bromeliaceae). Heredity 101:285–296

    PubMed  Google Scholar 

  • Barbará T, Martinelli G, Palma-Silva C, Fay MF, Mayo S, Lexer C (2009) Genetic relationships and variation in reproductive strategies in four closely related bromeliads adapted to neotropical ‘inselbergs’: Alcantarea glaziouana, A. regina, A. geniculata and A. imperialis (Bromeliaceae). Ann Bot 103:65–77

    PubMed  PubMed Central  Google Scholar 

  • Barbosa AR (2011) Biossistemática do complexo Vellozia hirsuta (Velloziaceae) baseada em análise filogeográfica e genética de populações. MSc Dissertation, Universidade Federal de Minas Gerais

    Google Scholar 

  • Barbosa NPU, Fernandes GW, Carneiro MAA, Júnior LA (2010) Distribution of non-native invasive species and soil properties in proximity to paved roads and unpaved roads in a quartzitic mountainous grassland of southeastern Brazil (rupestrian fields). Biol Invasions 12:3745–3755

    Google Scholar 

  • Barbosa AR, Fiorini CF, Silva-Pereira V, Mello-Silva R, Borba EL (2012) Geographical genetic structuring and phenotypic variation in the Vellozia hirsuta (Velloziaceae) ochlospecies complex. Am J Bot 99:1477–1488

    PubMed  Google Scholar 

  • Barbosa NPU, Fernandes GW, Sanchez-Azofeifa A (2015) A relict species restricted to a quartzitic mountain in tropical America: an example of microrefugium? Acta Bot Bras 29:299–309

    Google Scholar 

  • Barnard-Kubow KB, So N, Galloway LF (2016) Cytonuclear incompatibility contributes to the early stages of speciation. Evolution 70:2752–2766

    CAS  PubMed  Google Scholar 

  • Barreto HN, Varajão CA, Braucher R, Bourlès DL, Salgado AA, Varajão AF (2013) Denudation rates of the Southern Espinhaço Range, Minas Gerais, Brazil, determined by in situ-produced cosmogenic beryllium-10. Geomorphology 191:1–13

    Google Scholar 

  • Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67

    Google Scholar 

  • Bertorelle G, Benazzo A, Mona S (2010) ABC as a flexible framework to estimate demography over space and time: some cons, many pros. Mol Ecol 19:2609–2625

    CAS  PubMed  Google Scholar 

  • BFG (2015) Growing knowledge: an overview of Seed Plant diversity in Brazil. Rodriguésia 66:1085–1113

    Google Scholar 

  • Bonatelli IA, Perez MF, Peterson AT, Taylor NP, Zappi DC, Machado MC, Koch I, Pires AHC, Moraes EM (2014) Interglacial microrefugia and diversification of a cactus species complex: phylogeography and palaeodistributional reconstructions for Pilosocereus aurisetus and allies. Mol Ecol 23:3044–3063

    CAS  PubMed  Google Scholar 

  • Bond WJ, Midgley JJ (2001) Ecology of sprouting in woody plants: the persistence niche. Trends Ecol Evol 16:45–51

    CAS  PubMed  Google Scholar 

  • Borba EL, Felix JM, Semir J, Solferini VN (2000) Pleurothallis fabiobarrosii, a new Brazilian species: morphological and genetic data with notes on the taxonomy of Brazilian rupicolous Pleurothallis. Lindleyana 15:2–9

    Google Scholar 

  • Borba EL, Felix JM, Solferini VN, Semir J (2001a) Fly-pollinated Pleurothallis (Orchidaceae) species have high genetic variability: evidence from isozyme markers. Am J Bot 88:419–428

    CAS  PubMed  Google Scholar 

  • Borba EL, Trigo JR, Semir J (2001b) Variation of diastereoisomeric pyrrolizidine alkaloids in Pleurothallis (Orchidaceae). Biochem Syst Ecol 29:45–52

    CAS  PubMed  Google Scholar 

  • Borba EL, Funch RR, Ribeiro PL, Smidt EC, Silva-Pereira V (2007a) Demography, and genetic and morphological variability of the endangered Sophronitis sincorana (Orchidaceae) in the Chapada Diamantina, Brazil. Plant Syst Evol 267:129–146

    Google Scholar 

  • Borba EL, Funch RR, Ribeiro PL, Smidt EC, Silva-Pereira V (2007b) Demografia, variabilidade genética e morfológica e conservação de Cattleya tenuis (Orchidaceae), espécie ameaçada de extinção da Chapada Diamantina. Sitientibus Ser Ci Biol 7:211–222

    Google Scholar 

  • Byrne M, Hopper SD (2008) Granite outcrops as ancient islands in old landscapes: evidence from the phylogeography and population genetics of Eucalyptus caesia (Myrtaceae) in Western Australia. Biol J Linn Soc 93(1):177–188

    Google Scholar 

  • Carlucci MB, Bastazini VA, Hofmann GS, de Macedo JH, Iob G, Duarte LD, Hartz S, Müller SC (2015) Taxonomic and functional diversity of woody plant communities on opposing slopes of inselbergs in southern Brazil. Plant Ecol Divers 8:187–197

    Google Scholar 

  • Carmo FF, Jacobi CM (2016) Diversity and plant trait-soil relationships among rock outcrops in the Brazilian Atlantic rainforest. Plant Soil 403:7–20

    Google Scholar 

  • Carmo FF, Kamino LHY (2015) Geossistemas ferruginosos do Brasil: áreas prioritárias para conservação da diversidade geológica e biológica, patrimônio cultural e serviços ambientais. 3i Editora, Belo Horizonte

    Google Scholar 

  • Carmo FF, de Campos IC, Jacobi CM (2016) Effects of fine-scale surface heterogeneity on rock outcrop plant community structure. J Veg Sci 27:50–59

    Google Scholar 

  • Carmo FF, da Mota RC, Kamino LHY, Jacobi CM (2018) Check-list of vascular plant communities on ironstone ranges of south-eastern Brazil: dataset for conservation. Biodiv Data J 6:e27032. https://doi.org/10.3897/BDJ.6.e27032

    Article  Google Scholar 

  • Cavallari MM, Forzza RC, Veasey EA, Zucchi MI, Oliveira GCX (2006) Genetic variation in three endangered species of Encholirium (Bromeliaceae) from Cadeia do Espinhaço, Brazil, setected using RAPD markers. Biodivers Conserv 15:4357–4373

    Google Scholar 

  • Christenhusz MJ, Byng JW (2016) The number of known plants species in the world and its annual increase. Phytotaxa 261:201–217

    Google Scholar 

  • Collevatti RG, Rabelo SG, Vieira RF (2009) Phylogeography and disjunct distribution in Lychnophora ericoides (Asteraceae), an endangered cerrado shrub species. Ann Bot 104:655–664

    PubMed  PubMed Central  Google Scholar 

  • Collevatti RG, Castro TG, Lima JS, Telles MPC (2012) Phylogeography of Tibouchina papyrus (Pohl) Toledo (Melastomataceae), an endangered tree species from rocky savannas, suggests bidirectional expansion due to climate cooling in the Pleistocene. Ecol Evol 2:1024–1035

    PubMed  PubMed Central  Google Scholar 

  • Colwell RK, Brehm G, Cardelús CL, Gilman AC, Longino JT (2008) Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322:258–261

    CAS  PubMed  Google Scholar 

  • Conan Doyle A (1912) The lost world. Oxford University Press, Oxford

    Google Scholar 

  • Conceição ADS, Queiroz LP, Lambert SM, Pereira ACS, Borba EL (2008) Biosystematics of Chamaecrista sect. Absus subsect. Baseophyllum (Leguminosae-Caesalpinioideae) based on allozyme and morphometric analyses. Plant Syst Evol 270:183–207

    Google Scholar 

  • Cowling RM, Rundel PW, Lamont BB, Arroyo MK, Arianoutsou M (1996) Plant diversity in Mediterranean-climate regions. Trends Ecol Evol 11:362–366

    CAS  PubMed  Google Scholar 

  • Cowling RM, Potts AJ, Bradshaw PL, Colville J, Arianoutsou M, Ferrier S, Forest F, Fyllas NM, Hopper SD, Ojeda F, Procheş Ş, Smith RJ, Rundel PW, Vassilakis E, Zutta BR (2015) Variation in plant diversity in Mediterranean-climate ecosystems: the role of climatic and topographical stability. J Biogeogr 42:552–564

    Google Scholar 

  • Crawford DJ, Archibald JK (2017) Island floras as model systems for studies of plant speciation: prospects and challenges. J Syst Evol 55:1–15

    Google Scholar 

  • Crespi B, Nosil P (2013) Conflictual speciation: species formation via genomic conflict. Trends Ecol Evol 28:48–57

    PubMed  Google Scholar 

  • da Cruz DT, Selbach-Schnadelbach A, Lambert SM, Ribeiro PL, Borba EL (2011) Genetic and morphological variability in Cattleya elongata Barb. Rodr. (Orchidaceae), endemic to the campo rupestre vegetation in northeastern Brazil. Plant Syst Evol 294:87. https://doi.org/10.1007/s00606-011-0444-0

    Article  Google Scholar 

  • da Silva RM, Fernandes GW, Lovato MB (2007) Genetic variation in two Chamaecrista species (Leguminosae), one endangered and narrowly distributed and another widespread in the Serra do Espinhaço, Brazil. Can J Bot 85:629–636

    Google Scholar 

  • Dayrell RL, Arruda AJ, Buisson E, Silveira FAO (2016) Overcoming challenges on using native seeds for restoration of megadiverse resource-poor environments: a reply to Madsen et al. Restor Ecol 24(6):710–713

    Google Scholar 

  • de Oliveira MM, Dickman R (2017) The advantage of being slow: the quasi-neutral contact process. PLoS One 12(8):e0182672. https://doi.org/10.1371/journal.pone.0182672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Paula LF, Negreiros D, Azevedo LO, Fernandes RL, Stehmann JR, Silveira FAO (2015) Functional ecology as a missing link for conservation of a resource-limited flora in the Atlantic forest. Biodivers Conserv 24:2239–2253

    Google Scholar 

  • de Paula LF, Forzza RC, Neri AV, Bueno ML, Porembski S (2016) Sugar Loaf Land in south-eastern Brazil: a centre of diversity for mat-forming bromeliads on inselbergs. Bot J Linn Soc 181:459–476

    Google Scholar 

  • Duputié A, Delêtre M, De Granville JJ, McKey D (2009) Population genetics of Manihot esculenta ssp. flabellifolia gives insight into past distribution of xeric vegetation in a postulated forest refugium area in northern Amazonia. Mol Ecol 18:2897–2907

    PubMed  Google Scholar 

  • Echternacht L, Trovó M, Oliveira CT, Pirani JR (2011) Areas of endemism in the Espinhaço range in Minas Gerais, Brazil. Flora 206:782–791

    Google Scholar 

  • Ehrlén J, van Groenendael JM (1998) The trade-off between dispersability and longevity: an important aspect of plant species diversity. Appl Veg Sci 1:29–36

    Google Scholar 

  • Ellegren H (2014) Genome sequencing and population genomics in non-model organisms. Trends Ecol Evol 29:51–63

    PubMed  Google Scholar 

  • Feres F, Zucchi MI, de Souza AP, do Amaral MDCE, Bittrich V (2009) Phylogeographic studies of Brazilian “campo-rupestre” species: Wunderlichia mirabilis Riedel ex Baker (Asteraceae). Biotemas 22:17–26

    Google Scholar 

  • Fernandes GW (ed) (2016) Ecology and conservation of mountaintop grasslands in Brazil. Springer, Cham

    Google Scholar 

  • Fernandes GW, Barbosa NPU, Alberton B, Barbieri A, Dirzo R, Goulart F, Guerra TJ, Solar RRC (2018) The deadly route to collapse and the uncertain fate of Brazilian rupestrian grasslands. Biodivers Conserv 27:2587–2603

    Google Scholar 

  • Fiedler P (2015) The fascinating ecology of two megadiverse southern hemisphere ecosystems. Conserv Biol 29:1727–1729

    Google Scholar 

  • Fitzsimons JA, Michael DR (2017) Rocky outcrops: a hard road in the conservation of critical habitats. Biol Conserv 211:36–44

    Google Scholar 

  • Franceschinelli EV, Jacobi CM, Drummond MG, Resende MFS (2006) The genetic diversity of two Brazilian Vellozia (Velloziaceae) with different patterns of spatial distribution and pollination biology. Ann Bot 97:585–592

    CAS  PubMed  PubMed Central  Google Scholar 

  • Freitas L, Sazima M (2006) Pollination biology in a tropical high-altitude grassland in Brazil: interactions at the community level. Ann Mo Bot Gard 93:465–516

    Google Scholar 

  • Gentry AH (1982) Patterns of neotropical plant species diversity. Evol Biol 15:1–84

    Google Scholar 

  • Giannini TC, Giulietti AM, Harley RM, Viana PL, Jaffe R, Alves R et al (2017) Selecting plant species for practical restoration of degraded lands using a multiple-trait approach. Austral Ecol 42:510–521

    Google Scholar 

  • Giulietti AM, Pirani JR (1988) Patterns of geographic distribution of some plant species from the Espinhaço Range, Minas Gerais and Bahia, Brazil. In: Heyer WR, Vanzolini PE (eds) Proceedings of a workshop on Neotropical distribution pattern. Academia Brasileira de Ciências, Rio de Janeiro, pp 39–69

    Google Scholar 

  • Giulietti AM, Pirani JR, Harley RM (1997) Espinhaço range region. Eastern Brazil. In: Davis SD, Heywood VH, Herrera-MacBryde O, Villa-Lobos J, Hamilton AC (eds) Centres of plant diversity. A guide and strategies for the conservation, vol 3. The Americas. WWF/IUCN, Cambridge, pp 397–404

    Google Scholar 

  • Givnish TJ, Barfuss MH, Van Ee B, Riina R, Schulte K, Horres R et al (2014) Adaptive radiation, correlated and contingent evolution, and net species diversification in Bromeliaceae. Mol Phylogenet Evol 71:55–78

    PubMed  Google Scholar 

  • Gomes V, Collevatti RG, Silveira FAO, Fernandes GW (2004) The distribution of genetic variability in Baccharis concinna (Asteraceae), an endemic, dioecious and threatened shrub of rupestrian fields of Brazil. Conserv Genet 5:157–165

    CAS  Google Scholar 

  • Gomes VM, Negreiros D, Fernandes GW, Pires ACV, Silva ACDR, Le Stradic S (2018) Long-term monitoring of shrub species translocation in degraded Neotropical mountain grassland. Restor Ecol 26:91–96

    Google Scholar 

  • Gomes-da-Silva J, Amorim AM, Forzza RC (2017) Distribution of the xeric clade species of Pitcairnioideae (Bromeliaceae) in South America: a perspective based on areas of endemism. J Biogeogr 44:1994–2006

    Google Scholar 

  • Gonçalves-Oliveira RC, Wöhrmann T, Benko-Iseppon AM, Krapp F, Alves M, Wanderley MDGL, Weising K (2017) Population genetic structure of the rock outcrop species Encholirium spectabile (Bromeliaceae): the role of pollination vs. seed dispersal and evolutionary implications. Am J Bot 104:868–878

    PubMed  Google Scholar 

  • Götzenberger L, de Bello F, Bråthen KA, Davison J, Dubuis A, Guisan A et al (2012) Ecological assembly rules in plant communities—approaches, patterns and prospects. Biol Rev 87:111–127

    PubMed  Google Scholar 

  • Gradim C, Roncato J, Pedrosa-Soares AC, Cordani U, Dussin I, Alkmim FF, Queiroga G, Jacobsohn T, da Silva LC, Babinski M (2014) The hot back-arc zone of the Araçuaí orogen, Eastern Brazil: from sedimentation to granite generation. Braz J Geol 44:155–180

    Google Scholar 

  • Greiner S, Bock R (2013) Tuning a ménage à trois: co-evolution and co-adaptation of nuclear and organellar genomes in plants. BioEssays 35:354–365

    CAS  PubMed  Google Scholar 

  • Greiner S, Rauwolf UWE, Meurer J, Herrmann RG (2011) The role of plastids in plant speciation. Mol Ecol 20:671–691

    PubMed  Google Scholar 

  • Güsewell S, Schroth MH (2017) How functional is a trait? Phosphorus mobilization through root exudates differs little between Carex species with and without specialized dauciform roots. New Phytol 215:1438–1450

    PubMed  Google Scholar 

  • Hamrick JL, Godt MJW (1990) Allozyme diversity in plant species. In: Brown AHD, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding and genetic resources. Sinauer, Sunderland, MA, pp 43–63

    Google Scholar 

  • Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc B 351(1345):1291–1298

    Google Scholar 

  • Hmeljevski KV, Wolowski M, Forzza RC, Freitas L (2017a) High outcrossing rates and short-distance pollination in a species restricted to granitic inselbergs. Aust J Bot 65:315–326

    Google Scholar 

  • Hmeljevski KV, Nazareno AG, Bueno ML, dos Reis MS, Forzza RC (2017b) Do plant populations on distinct inselbergs talk to each other? A case study of genetic connectivity of a bromeliad species in an Ocbil landscape. Ecol Evol 7:4704–4716

    PubMed  PubMed Central  Google Scholar 

  • Hoorn C, Perrigo A, Antonelli A (2018) Mountains, climate and biodiversity: an introduction. In: Hoorn C, Perrigo A, Antonelli A (eds) Mountains, climate and biodiversity. Wiley, Chichester, pp 1–14

    Google Scholar 

  • Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant Soil 322:49–86

    CAS  Google Scholar 

  • Hopper SD (2018) Natural hybridization in the context of Ocbil theory. S Afr J Bot 118:284289

    Google Scholar 

  • Hopper SD, Silveira FAO, Fiedler PL (2016) Biodiversity hotspots and Ocbil theory. Plant Soil 403:167–216

    CAS  Google Scholar 

  • Hughes C, Eastwood R (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc Natl Acad Sci USA 103(27):10334–10339

    CAS  PubMed  Google Scholar 

  • Hughes CE, Pennington RT, Antonelli A (2013) Neotropical plant evolution: assembling the big picture. Bot J Linn Soc 171:1–18

    Google Scholar 

  • Iganci JR, Heiden G, Miotto STS, Pennington RT (2011) Campos de Cima da Serra: the Brazilian subtropical highland grasslands show an unexpected level of plant endemism. Bot J Linn Soc 167:378–393

    Google Scholar 

  • Inglis PW, Cavalcanti TB (2018) A molecular phylogeny of the genus Diplusodon (Lythraceae), endemic to the campos rupestres and cerrados of South America. Taxon 67:66–82

    Google Scholar 

  • Jacobi CM, Carmo FF, Vincent RC, Stehmann JR (2007) Plant communities on ironstone outcrops: a diverse and endangered Brazilian ecosystem. Biodivers Conserv 16:2185–2200

    Google Scholar 

  • Jaffé R, Prous X, Calux A, Gastauer M, Nicacio G, Zampaulo R, Souza-Filho PWM, Oliveira G, Brandi IV, Siqueira JO (2018) Conserving relics from ancient underground worlds: assessing the influence of cave and landscape features on obligate iron cave dwellers from the Eastern Amazon. PeerJ 6:e4531. https://doi.org/10.7717/peerj.4531

    Article  PubMed  PubMed Central  Google Scholar 

  • Jesus FF, Solferini VN, Semir J, Prado PI (2001) Local genetic differentiation in Proteopsis argentea (Asteraceae), a perennial herb endemic in Brazil. Plant Syst Evol 226:59–68

    CAS  Google Scholar 

  • Jesus FF, Abreu AG, Semir J, Solferini VN (2009) Low genetic diversity but local genetic differentiation in endemic Minasia (Asteraceae) species from Brazil. Plant Syst Evol 277:187–196

    Google Scholar 

  • Khan G, Ribeiro PM, Bonatelli IA, Perez MF, Franco FF, Moraes EM (2018) Weak population structure and no genetic erosion in Pilosocereus aureispinus: a microendemic and threatened cactus species from eastern Brazil. PLoS One 13(4):e0195475. https://doi.org/10.1371/journal.pone.0195475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kier G, Mutke J, Dinerstein E, Ricketts TH, Küper W, Kreft H, Barthlott W (2005) Global patterns of plant diversity and floristic knowledge. J Biogeogr 32:1107–1116

    Google Scholar 

  • Kier G, Kreft H, Lee TM, Jetz W, Ibisch PL, Nowicki C, Mutke J, Barthlott W (2009) A global assessment of endemism and species richness across island and mainland regions. Proc Natl Acad Sci USA 106(23):9322–9327

    CAS  PubMed  Google Scholar 

  • Klein C (2005) Some Precambrian banded iron-formation (BIFs) from around the world: their age, geologic setting, mineralogy, metamorphism, geochemistry, and origin. Am Mineral 90:1473–1499

    CAS  Google Scholar 

  • Krüger M, Teste FP, Laliberté E, Lambers H, Coghlan M, Zemunik G, Bunce M (2015) The rise and fall of arbuscular mycorrhizal fungal diversity during ecosystem retrogression. Mol Ecol 24:4912–4930

    PubMed  Google Scholar 

  • Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103

    PubMed  Google Scholar 

  • Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 348:7–27

    Google Scholar 

  • Lambers H, Albornoz F, Kotula L, Laliberté E, Ranathunge K, Teste FP, Zemunik G (2018) How belowground interactions contribute to the coexistence of mycorrhizal and non-mycorrhizal species in severely phosphorus-impoverished hyperdiverse ecosystems. Plant Soil 424:11–33

    CAS  Google Scholar 

  • Lambert SM, Borba EL, Machado MC (2006a) Allozyme diversity and morphometrics of the endangered Melocactus glaucescens (Cactaceae), and investigation of the putative hybrid origin of Melocactus × albicephalus (Melocactus ernestii × M. glaucescens) in north-eastern Brazil. Plant Species Biol 21:93–108

    Google Scholar 

  • Lambert SM, Borba EL, Machado MC, Andrade SCDS (2006b) Allozyme diversity and morphometrics of Melocactus paucispinus (Cactaceae) and evidence for hybridization with M. concinnus in the Chapada Diamantina, north-eastern Brazil. Ann Bot 97:389–403

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lanes ÉC, Pope NS, Alves R, Carvalho Filho NM, Giannini TC, Giulietti AM et al (2018) Landscape genomic conservation assessment of a narrow-endemic and a widespread morning glory from Amazonian savannas. Front Plant Sci 9(532). https://doi.org/10.3389/fpls.2018.00532

  • Lavor P, van den Berg C, Jacobi CM, Carmo FF, Versieux LM (2014) Population genetics of the endemic and endangered Vriesea minarum (Bromeliaceae) in the Iron Quadrangle, Espinhaço Range, Brazil. Am J Bot 101:1167–1175

    PubMed  Google Scholar 

  • Le Stradic S, Buisson E, Fernandes GW (2015) Vegetation composition and structure of some Neotropical mountain grasslands in Brazil. J Mt Sci 12:864–877

    Google Scholar 

  • Le Stradic S, Fernandes GW, Buisson E (2018) No recovery of campo rupestre grasslands after gravel extraction: implications for conservation and restoration. Restor Ecol 26(S2):S151–S159

    Google Scholar 

  • Leal BS, Chaves CJ, Koehler S, Borba EL (2016) When hybrids are not hybrids: a case study of a putative hybrid zone between Cattleya coccinea and C. brevipedunculata (Orchidaceae). Bot J Linn Soc 181:621–639

    Google Scholar 

  • Leles B, Chaves AV, Russo P, Batista JA, Lovato MB (2015) Genetic structure is associated with phenotypic divergence in floral traits and reproductive investment in a high-altitude orchid from the Iron Quadrangle, southeastern Brazil. PLoS One 10(3):e0120645. https://doi.org/10.1371/journal.pone.0120645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loeuille B, Semir J, Lohmann LG, Pirani JR (2015) A phylogenetic analysis of Lychnophorinae (Asteraceae: Vernonieae) based on molecular and morphological data. Syst Bot 40:299–315

    Google Scholar 

  • Lousada JM, Borba EL, Ribeiro KT, Ribeiro LC, Lovato MB (2011) Genetic structure and variability of the endemic and vulnerable Vellozia gigantea (Velloziaceae) associated with the landscape in the Espinhaço Range, in southeastern Brazil: implications for conservation. Genetica 139:431–440

    PubMed  Google Scholar 

  • Lousada JM, Lovato MB, Borba EL (2013) High genetic divergence and low genetic variability in disjunct populations of the endemic Vellozia compacta (Velloziaceae) occurring in two edaphic environments of Brazilian campos rupestres. Braz J Bot 36:45–53

    Google Scholar 

  • Madriñán S, Cortés AJ, Richardson JE (2013) Páramo is the world’s fastest evolving and coolest biodiversity hotspot. Front Genet 4(192). https://doi.org/10.3389/fgene.2013.00192

  • Main BY (1997) Granite outcrops: a collective ecosystem. J R Soc West Aust 80:113–122

    Google Scholar 

  • Martin LJ, Blossey B, Ellis E (2012) Mapping where ecologists work: biases in the global distribution of terrestrial ecological observations. Front Ecol Environ 10:195–201

    Google Scholar 

  • Martinelli G (1989) Campos de altitude. Editora Index, Rio de Janeiro

    Google Scholar 

  • McCormack JE, Huang H, Knowles LL (2009) Sky islands. In: Gillespie R, Clague D (eds) Encyclopedia of islands. University of California Press, Berkeley, CA, pp 841–843

    Google Scholar 

  • Moraes EM, Abreu AG, Andrade SC, Sene FM, Solferini VN (2005) Population genetic structure of two columnar cacti with a patchy distribution in eastern Brazil. Genetica 125:311–323

    PubMed  Google Scholar 

  • Moreira RG, McCauley RA, Cortés-Palomec AC, Fernandes GW, Oyama K (2010) Spatial genetic structure of Coccoloba cereifera (Polygonaceae), a critically endangered microendemic species of Brazilian rupestrian fields. Conserv Genet 11:1247–1255

    CAS  Google Scholar 

  • Morellato LPC, Silveira FAO (2018) Plant life in campo rupestre: new lessons from an ancient biodiversity hotspot. Flora 238:1–10

    Google Scholar 

  • Mucina L (2018) Vegetation of Brazilian campos rupestres on siliceous substrates and their global analogues. Flora 238:11–23

    Google Scholar 

  • Mucina L, Wardell-Johnson GW (2011) Landscape age and soil fertility, climatic stability, and fire regime predictability: beyond the OCBIL framework. Plant Soil 341:1–23

    CAS  Google Scholar 

  • Murphy BP, Bowman DM (2012) What controls the distribution of tropical forest and savanna? Ecol Lett 15:748–758

    PubMed  Google Scholar 

  • Negreiros D, Le Stradic S, Fernandes GW, Rennó HC (2014) CSR analysis of plant functional types in highly diverse tropical grasslands of harsh environments. Plant Ecol 215:379–388

    Google Scholar 

  • Neves DM, Dexter KG, Pennington RT, Valente AS, Bueno ML, Eisenlohr PV et al (2017) Dissecting a biodiversity hotspot: the importance of environmentally marginal habitats in the Atlantic Forest Domain of South America. Divers Distrib 23:898–909

    Google Scholar 

  • Neves DM, Dexter KG, Pennington RT, Bueno ML, de Miranda PL, Oliveira-Filho AT (2018) Lack of floristic identity in campos rupestres—a hyperdiverse mosaic of rocky montane savannas in South America. Flora 238:24–31

    Google Scholar 

  • Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155

    CAS  PubMed  Google Scholar 

  • Oliveira RS, Galvão HC, de Campos MC, Eller CB, Pearse SJ, Lambers H (2015) Mineral nutrition of campos rupestres plant species on contrasting nutrient-impoverished soil types. New Phytol 205:1183–1194

    CAS  PubMed  Google Scholar 

  • Overbeck GE, Vélez-Martin E, Scarano FR, Lewinsohn TM, Fonseca CR, Meyer ST, Müller SC, Ceotto P, Dadalt L, Durigan G, Ganade G, Gossner MM, Guadagnin DL, Lorenzen K, Jacobi CM, Weisser WW, Pillar VD (2015) Conservation in Brazil needs to include non-forest ecosystems. Divers Distrib 21:1455–1460

    Google Scholar 

  • Paggi GM, Sampaio JAT, Bruxel M, Zanella CM, Goeetze M, Buettow MV, Palma-Silva C, Bered F (2010) Seed dispersal and population structure in Vriesea gigantea, a bromeliad from the Brazilian Atlantic Rainforest. Bot J Linn Soc 164:317–325

    Google Scholar 

  • Palma-Silva C, Wendt T, Pinheiro F, Barbará T, Fay MF, Cozzolino S, Lexer C (2011) Sympatric bromeliad species (Pitcairnia spp.) facilitate tests of mechanisms involved in species cohesion and reproductive isolation in Neotropical inselbergs. Mol Ecol 20:3185–3201

    CAS  PubMed  Google Scholar 

  • Patiño J, Whittaker RJ, Borges PA, Fernández-Palacios JM, Ah-Peng C, Araújo MB et al (2017) A roadmap for island biology: 50 fundamental questions after 50 years of The Theory of Island Biogeography. J Biogeogr 44:963–983

    Google Scholar 

  • Pereira ACS, Borba EL, Giulietti AM (2007) Genetic and morphological variability of the endangered Syngonanthus mucugensis Giul. (Eriocaulaceae) from the Chapada Diamantina, Brazil: implications for conservation and taxonomy. Bot J Linn Soc 153:401–416

    Google Scholar 

  • Perez MF, Bonatelli IAS, Moraes EM, Carstens BC (2016a) Model-based analysis supports interglacial refugia over long-dispersal events in the diversification of two South American cactus species. Heredity 116:550–557

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perez MF, Carstens BC, Rodrigues GL, Moraes EM (2016b) Anonymous nuclear markers reveal taxonomic incongruence and long-term disjunction in a cactus species complex with continental-island distribution in South America. Mol Phylogenet Evol 95:11–19

    PubMed  Google Scholar 

  • Pianka ER (1966) Latitudinal gradients in species diversity: a review of concepts. Am Nat 100(910):33–46

    Google Scholar 

  • Pierce S, Negreiros D, Cerabolini BE, Kattge J, Díaz S, Kleyer M et al (2017) A global method for calculating plant CSR ecological strategies applied across biomes world-wide. Funct Ecol 31:444–457

    Google Scholar 

  • Pinheiro F, de Barros F, Palma-Silva C, Fay MF, Lexer C, Cozzolino S (2011) Phylogeography and genetic differentiation along the distributional range of the orchid Epidendrum fulgens: a Neotropical coastal species not restricted to glacial refugia. J Biogeogr 38:1923–1935

    Google Scholar 

  • Pinheiro F, Cozzolino S, Draper D, de Barros F, Félix LP, Fay MF, Palma-Silva C (2014) Rock outcrop orchids reveal the genetic connectivity and diversity of inselbergs of northeastern Brazil. BMC Evol Biol 14:49. https://doi.org/10.1186/1471-2148-14-49

    Article  PubMed  PubMed Central  Google Scholar 

  • Pontara V, Bueno ML, Rezende VL, de Oliveira-Filho AT, Gastauer M, Meira-Neto JAA (2018) Evolutionary history of campo rupestre: an approach for conservation of woody plant communities. Biodivers Conserv 27:2877–2896

    Google Scholar 

  • Poot P, Hopper SD, van Diggelen JM (2012) Exploring rock fissures: does a specialized root morphology explain endemism on granite outcrops? Ann Bot 110:291–300

    PubMed  PubMed Central  Google Scholar 

  • Porembski S (2000) The invasibility of tropical granite outcrops (‘inselbergs’) by exotic weeds. J R Soc West Aust 83:131–134

    Google Scholar 

  • Porembski S (2007) Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Braz J Bot 30:579–586

    Google Scholar 

  • Porembski S, Barthlott W (2000) Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccation-tolerant vascular plants. Plant Ecol 151:19–28

    Google Scholar 

  • Porembski S, Seine R, Barthlott W (1997) Inselberg vegetation and the biodiversity of granite outcrops. J R Soc West Aust 80:193–199

    Google Scholar 

  • Porembski S, Silveira FAO, Fiedler PL, Watve A, Rabarimanarivo M, Kouame F, Hopper SD (2016) Worldwide destruction of inselbergs and related rock outcrops threatens a unique ecosystem. Biodivers Conserv 25:2827–2830

    Google Scholar 

  • Potter PE, Szatmari P (2009) Global Miocene tectonics and the modern world. Earth-Sci Rev 96:279–295

    Google Scholar 

  • Rando JG, Zuntini AR, Conceição AS, van den Berg C, Pirani JR, de Queiroz LP (2016) Phylogeny of Chamaecrista ser. Coriaceae (Leguminosae) unveils a lineage recently diversified in Brazilian campo rupestre vegetation. Int J Plant Sci 177:3–17

    Google Scholar 

  • Rangel TF, Edwards NR, Holden PB, Diniz-Filho JAF, Gosling WD, Coelho MTP, Cassemiro FAS, Rahbek C, Colwell RK (2018) Modeling the ecology and evolution of biodiversity: biogeographical cradles, museums, and graves. Science 361(6399):eaar5452. https://doi.org/10.1126/science.aar5452

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro PL, Borba EL, Smidt EC, Lambert SM, Selbach-Schnadelbach AS, van den Berg C (2008) Genetic and morphological variation in the Bulbophyllum exaltatum (Orchidaceae) complex occurring in the Brazilian “campos rupestres”: implications for taxonomy and biogeography. Plant Syst Evol 270:109–137

    Google Scholar 

  • Ribeiro PCC, Pinheiro LC, Domingues R, Forzza RC, Machado MA, Viccini LF (2013) Genetic diversity of Vriesea cacuminis (Bromeliaceae): an endangered and endemic Brazilian species. Genet Mol Res 12:1934–1943

    CAS  PubMed  Google Scholar 

  • Ribeiro PL, Pereira ACS, Borba EL, Giulietti AM (2018) Genetic and morphological diversity and evidence of hybridization in the “sempre-vivas” (Comanthera, Eriocaulaceae) endemic to the Chapada Diamantina, Bahia, Brazil. Flora 238:60–71

    Google Scholar 

  • Richardson JE, Pennington RT, Pennington TD, Hollingsworth PM (2001) Rapid diversification of a species-rich genus of neotropical rain forest trees. Science 293(5538):2242–2245

    CAS  PubMed  Google Scholar 

  • Rull V (2005) Biotic diversification in the Guayana highlands: a proposal. J Biogeogr 32:921–927

    Google Scholar 

  • Rull V (2009) Pantepui. In: Gillespie R, Clague D (eds) Encyclopedia of islands. University of California Press, Berkeley, CA, pp 717–720

    Google Scholar 

  • Saadi A (1995) A geomorfologia da Serra do Espinhaço em Minas Gerais e de suas margens. Rev Geonomos 3:41–63

    Google Scholar 

  • Safford HD (1999a) Brazilian Páramos I. An introduction to the physical environment and vegetation of the campos de altitude. J Biogeogr 26:693–712

    Google Scholar 

  • Safford HD (1999b) Brazilian Páramos II. Macro-and mesoclimate of the campos de altitude and affinities with high mountain climates of the tropical Andes and Costa Rica. J Biogeogr 26:713–737

    Google Scholar 

  • Sarthou C, Samadi S, Boisselier-Dubayle MC (2001) Genetic structure of the saxicole Pitcairnia geyskesii (Bromeliaceae) on inselbergs in French Guiana. Am J Bot 88:861–868

    CAS  PubMed  Google Scholar 

  • Sarthou C, Pavoine S, Gasc JP, De Massary JC, Ponge JF (2017) From inselberg to inselberg: floristic patterns across scales in French Guiana (South America). Flora 229:147–158

    Google Scholar 

  • Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. Ann Bot 90:517–524

    PubMed  PubMed Central  Google Scholar 

  • Schaefer CE, Corrêa GR, Candido HG, Arruda DM, Nunes JA, Araujo RW, Rodrigues PMS, Fernandes Filho EI, Pereira AFS, Brandão PC, Neri AV (2016) The physical environment of rupestrian grasslands (Campos Rupestres) in Brazil: geological, geomorphological and pedological characteristics, and interplays. In: Fernandes GW (ed) Ecology and conservation of mountaintop grasslands in Brazil. Springer, Cham, pp 15–53

    Google Scholar 

  • Schemske DW, Mittelbach GG (2017) “Latitudinal gradients in species diversity”: reflections on Pianka’s 1966 article and a look forward. Am Nat 189:599–603

    PubMed  Google Scholar 

  • Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353

    PubMed  Google Scholar 

  • Schut AG, Wardell-Johnson GW, Yates CJ, Keppel G, Baran I, Franklin SE, Hopper SD, Van Niel KP, Mucina L, Byrne M (2014) Rapid characterisation of vegetation structure to predict refugia and climate change impacts across a global biodiversity hotspot. PLoS One 9(1):e82778. https://doi.org/10.1371/journal.pone.0082778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva JB, Sfair JC, dos Santos ND, Pôrto KC (2018) Different trait arrangements can blur the significance of ecological drivers of community assembly of mosses from rocky outcrops. Flora 238:43–50

    Google Scholar 

  • Silveira FAO, Negreiros D, Barbosa NPU, Buisson E, Carmo FF, Carstensen DW, Conceição AA, Cornelissen TG, Echternacht L, Fernandes GW, Garcia QS, Guerra TJ, Jacobi CM, Lemos-Filho JP, Le Stradic S, Morellato LPC, Neves FS, Oliveira RS, Schaefer CE, Viana PL, Lambers H (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant Soil 403:129–152

    CAS  Google Scholar 

  • Steinbauer MJ, Field R, Grytnes JA, Trigas P, Ah-Peng C, Attorre F et al (2016) Topography-driven isolation, speciation and a global increase of endemism with elevation. Glob Ecol Biogeogr 25:1097–1107

    Google Scholar 

  • Stock WD, Pate JS, Kuo J, Hansen AP (1989) Resource control of seed set in Banksia laricina C. Gardner (Proteaceae). Funct Ecol 3:453–460

    Google Scholar 

  • Stuessy TF, Takayama K, López-Sepúlveda P, Crawford DJ (2014) Interpretation of patterns of genetic variation in endemic plant species of oceanic islands. Bot J Linn Soc 174:276–288

    PubMed  Google Scholar 

  • Tapper SL, Byrne M, Yates CJ, Keppel G, Hopper SD, Van Niel K, Schut AGT, Mucina L, Wardell-Johnson GW (2014a) Isolated with persistence or dynamically connected? Genetic patterns in a common granite outcrop endemic. Divers Distrib 20:987–1001

    Google Scholar 

  • Tapper SL, Byrne M, Yates CJ, Keppel G, Hopper SD, Van Niel K, Schut AGT, Mucina L, Wardell-Johnson GW (2014b) Prolonged isolation and persistence of a common endemic on granite outcrops in both mesic and semi-arid environments in south-western Australia. J Biogeogr 41:2032–2044

    Google Scholar 

  • Turner BL, Hayes PE, Laliberté E (2018) A climosequence of chronosequences in southwestern Australia. Eur J Soil Sci 69:69–85

    CAS  Google Scholar 

  • Twidale CR (1982) Granite landforms. Elsevier Scientific Publishing, Amsterdam

    Google Scholar 

  • Veldman JW, Overbeck GE, Negreiros D, Mahy G, Le Stradic S, Fernandes GW, Durigan G, Buisson E, Putz FE, Bond WJ (2015) Where tree planting and forest expansion are bad for biodiversity and ecosystem services. Bioscience 65:1011–1018

    Google Scholar 

  • Veldman JW, Silveira FAO, Fleischman FD, Ascarrunz NL, Durigan G (2017) Grassy biomes: an inconvenient reality for large-scale forest restoration? A comment on the essay by Chazdon and Laestadius. Am J Bot 104:649–651

    PubMed  Google Scholar 

  • Viana PL, Mota NFDO, Gil ADSB, Salino A, Zappi DC, Harley RM, Ilkiu-Borges AL, Secco RS, Almeida TE, Watanabe MTC, Santos JUM, Trovó M, Maurity C, Giulietti AM (2016) Flora of the cangas of the Serra dos Carajás, Pará, Brazil: history, study area and methodology. Rodriguésia 67:1107–1124

    Google Scholar 

  • Vieira BC, Salgado AAR, Santos LJC (eds) (2015) Landscapes and landforms of Brazil. Springer, London

    Google Scholar 

  • Villa PM, Gastauer M, Martins SV, Carrión JF, Campos PV, Rodrigues AC, Heringer G, Meira-Neto JAA (2018) Phylogenetic structure is determined by patch size in rock outcrop vegetation on an inselberg in the northern Amazon region. Acta Amazon 48:248–256

    Google Scholar 

  • Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19

    CAS  Google Scholar 

  • Zappi DC, Moro MF, Meagher TR, Lughadha EN (2017) Plant biodiversity drivers in Brazilian Campos Rupestres: insights from phylogenetic structure. Front Plant Sci 8:2141. https://doi.org/10.3389/fpls.2017.02141

    Article  PubMed  PubMed Central  Google Scholar 

  • Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat Plants 1(5):15050. https://doi.org/10.1038/NPLANTS.2015.50

    Article  CAS  Google Scholar 

Download references

Acknowledgements

FAOS thanks financial support from FAPEMIG and CNPq and support from Luiza C. Martins. RLCD received a scholarship from CAPES and a Scholarship for International Research Fees at UWA. CFF thanks financial support from CAPES and CNPq. ELB receives a scholarship from CNPq. Prof. S. D. Hopper provided criticism that improved the quality of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fernando A. O. Silveira .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Silveira, F.A.O., Dayrell, R.L.C., Fiorini, C.F., Negreiros, D., Borba, E.L. (2020). Diversification in Ancient and Nutrient-Poor Neotropical Ecosystems: How Geological and Climatic Buffering Shaped Plant Diversity in Some of the World’s Neglected Hotspots. In: Rull, V., Carnaval, A. (eds) Neotropical Diversification: Patterns and Processes. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-030-31167-4_14

Download citation

Publish with us

Policies and ethics