Skip to main content

Advertisement

SpringerLink
Log in

Taxus baccata in the Azores: a relict form at risk of imminent extinction

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Taxus baccata L., a Tertiary relict formerly widespread in the Azores Archipelago, was recently classified as “probably extinct”. This paper documents the persistence of the species in the Azores and provides its first characterization by means of morphometric and genetic analyses. Only five individuals were found, growing on Pico Island. Although the population size is critically small it retains some highly significant characteristics for the assessment of the genetic diversity of the species and its phylogeography. The leaves of the Azorean provenance were smaller than those of all other Taxus baccata described in literature; moreover, they have a higher stomata density and more numerous stomata rows. These features are all “primitive”, according to suggested morphological evolutionary trends. We assume that sequence analysis of the chloroplast trnS–trnQ intergenic spacer demonstrates that the Azorean population represents a different evolutionary line within Taxus. This suggests a more direct derivation from ancestors than provenances from Mediterranean and European regions. These individuals may be the last survivors of an ancient lineage, preserved in the Azores as part of the Macaronesian flora. Immediate conservation action focusing on site protection and ex situ reproduction strategies is recommended to save this lineage from imminent extinction.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Notes

  1. It has to be pointed out that the Azorean yew specimen described here presents clear differences with a not well circumstantiated var. variegata, described by Dempsey and Hook (2000); this latter is probably different from that of Spjut (2007b).

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Arruda V (2004) Caracterização climática das Ilhas do Faial e do Pico com base no modelo CIELO. Departamento de Ciências Agrárias. Angra do Heroísmo, Universidade dos Açores

  • Azevedo EB (1996) Modelação do Clima Insular à Escala Local. Modelo CIELO aplicado à Ilha Terceira. Departamento de Ciências Agrárias PhD thesis, Universidade dos Açores, Angra do Heroísmo

  • Azevedo EB, Pereira LS, Itier B (1999) Modelling the local climate in Islands environments: water balance applications. Agric Water Manage 40:393–403. doi:10.1016/S0378-3774(99)00012-8

    Article  Google Scholar 

  • Borges PAV, Cunha R, Gabriel R, Martins AMF, Silva L, Vieira V (eds) (2005) A list of the terrestrial fauna (Mollusca and Arthropoda) and flora (Bryophyta, Pteridaphyta and Spermatophyta) from the Azores. Direcção Regional do Ambiente and Universidade dos Açores, Horta, Angra do Heroísmo and Ponta Delgada

    Google Scholar 

  • Bramwell D, Richardson IBK (1973) Floristic connections between Macaronesia and the East Mediterranean Region. Monographiae Biologicae Canarienses N 4:118–125

    Google Scholar 

  • Brande A (2001) Die Eibe in Berlin einst und jetzt. Der Eibenfreund 8:24–43

    Google Scholar 

  • Capelo J, Sequeira M, Jardim R, Mesquita S (2007) Biologia e Ecologia das florestas das Ilhas–Madeira. In: Silva JS (ed) Árvores e Florestas de Portugal–Açores e Madeira, a floresta das ilhas. Público Comunicação Social, SA Lisboa, Portugal, pp 81–135. doi:10.1007/s00468-008-0251-6

    Google Scholar 

  • Cardoso PB, Borges PAV, Costa AC, Cunha RT, Gabriel R, Frias Martins AM, Silva L, Homem N, Martins M, Rodrigues P, Martins B, Mendonça E (2008) A perspectiva arquipelágica: Açores. In: Martin JL, Arechavaleta M, Borges PAV, Faria B (eds) As cem espécies ameaçadas prioritárias em termos de gestão na região europeia biogeográfica da Macaronésia. Consejería de Medio Ambiente y Ordenación Territorial, Gobierno de Canárias

    Google Scholar 

  • Carqueijeiro E, Silva HM, Santos R, Antunes A (2005) Áreas protegidas dos Açores. Secretaria Regional dos Açores, Horta

    Google Scholar 

  • Carracedo JC, Pérez Torrado FJ, Ancochea E, Meco J, Hérnan F, Cubas CR, Casillas R, Rodríguez Badiola E, Ahijado A (2002) Cenozoic volcanism II: the Canary Islands. In: Gibson W, Moreno T (eds) The geology of Spain. The Geological Society, London

    Google Scholar 

  • Ceballos L (1953) Macaronesia—Algunas consideraciones sobre la flora y vegetación forestal. Anais do Instituto Superior de Agronomia, pp 79–108

  • CLIMAAT (2009) Climate database, Angra do Heroísmo. http://www.climaat.angra.uac.pt. Retrieved 20 Feb 2009

  • Cope EA (1998) Taxaceae: the genera and cultivated species. Bot Rev 64(4):291–322. doi:10.1007/BF02857621

    Article  Google Scholar 

  • Cordeyro AP (1717) História Insulana das Ilhas a Portugal Sujeytas no Oceano Occidental. Secretaria Regional da Educação e Cultura (1981), Terceira, Angra do Heroísmo

  • Dempsey D, Hook I (2000) Yew (Taxus) species—chemical and morphological variations. Pharm biol (Formerly International Journal of Pharmacognosy) 38. doi: 10.1076/1388-0209(200009)38:4;1-A;FT274

  • Devillers P, Devillers-Terschuren J, Ledant JP (1991) CORINE biotopes manual. Habitats of the European community. Data specifications—Part 2. EUR 12587/3 EN. Commission of the European Commuties, Directorate–General Environment, Nuclear Safety and Civil Protection, Luxemburg

  • Dhar A, Ruprecht H, Vacik H (2008) Population viability risk management (PVRM) for in situ management of endangered tree species–A case study on a Taxus baccata L population. For Ecol Manag 255:2835–2845. doi:10.1016/j.foreco.2008.01.059

    Article  Google Scholar 

  • Di Sapio OA, Gattuso SJ, Gattuso MA (1997) Morphoanatomical characters of Taxus baccata bark and leaves. Fitoterapia 68(3):252–260

    Google Scholar 

  • Dias E (1996) Vegetação natural dos Açores. Ecologia e sintaxonomia das florestas naturais. PhD thesis, Universidade dos Açores, Angra do Heroísmo

  • Dias E, Pereira D, Medeiros V, Mendes J, Elias B (2007) Distribuição das principais manchas florestais: Açores. In: Silva JS (ed) Árvores e Florestas de Portugal vol 6: Açores e Madeira, a Floresta das Ilhas. Público/FLad, Lisbon

    Google Scholar 

  • Drouet H (1866) Catalogue de la Flore des Iles Açores. L’Itinéraire d’un voyage dans cet archipel. J-B Bailliére & Fils, Paris

    Google Scholar 

  • Drummond FF (1859) Annaes da Ilha Terceira. Câmara Municipal de Angra do Heroísmo, Angra do Heroísmo, Azores

    Google Scholar 

  • ETC./BD (2005) Natura 2000 unified site database (Special areas of conservation and special protected areas)—Taxus baccata factsheet. E. Commission, European topic centre on biological diversity—European environment agency

  • European Community (1992) Council directive 92/43/ECC, 21 May 1992 on the conservation of natural habitats and on wild fauna and flora. European Commission, Brussels

    Google Scholar 

  • Frutuoso G (1583) Saudades da Terra (6 vols). Ponta Delgada, Instituto Cultural de Ponta Delgada, 2005, Azores

  • Goodman J, Walsh V (2001) The story of Taxol: nature and politics in the pursuit of an anti-cancer drug. Cambridge University Press, Cambridge

    Google Scholar 

  • Guppy HB (1917) Plants, seeds and currents in the West Indies and Azores. Williams and Norgate, London

    Google Scholar 

  • Hageneder F (2007) Yew a history. Sutton Publishing, Stroud

    Google Scholar 

  • Hao DC, Huang B, Yang L (2008) Phylogenetic relationships of the genus Taxus inferred from chloroplast intergenic spacer and nuclear coding DNA. Biol Pharm Bull 31(2):260–265. doi:10.1248/bpb.31.260

    Article  CAS  Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913. doi:10.1038/35016000

    Article  CAS  PubMed  Google Scholar 

  • Hobohm C (2000) Plant species diversity and endemism on islands and archipelagos, with special reference to the Macaronesian Islands. Flora 195:9–24

    Google Scholar 

  • Humphries CJ (1979) Endemism and evolution in Macaronesia. Plants and Islands. D. Bramwell, London

    Google Scholar 

  • Iszkulo G, Jasinska AK, Giertych MJ, Boratynski A (2009) Do secondary sexual dimorphism and female intolerance to drought influence the sex ratio and extinction risk of Taxus baccata? Plant Ecol 200(2):229–240. doi:10.1007/s11258-008-9447-5

    Article  Google Scholar 

  • IUCN (2009) Red list of threatened species. Version 2009.1. http://www.iucnredlist.org. Cited on 4 Aug 2009

  • Karnovsky MJ (1965) A formaldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137A–138A

    Google Scholar 

  • Kim SCM, McGowen MR, Lubinsky P, Barber JC, Mort ME, Santos-Guerra A (2008) Timing and tempo of early and successive adaptive radiations in Macaronesia. PloS One 3(5). doi: 10.1371/journal.pone.0002139

  • Kimura M (1980) A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Macedo ALS (1871) História das quatro ilhas que formam o distrito da Horta, vols. I a III. Edição fac-similada de 1981, Região Autónoma dos Açores—SREC/DRAC, Angra do Heroísmo

  • Mai DH (1989) Development and regional differentiation of the European vegetation during the Tertiary. Pl Syst Evol 162:79–91. doi:10.1007/BF00936911

    Article  Google Scholar 

  • Mai DH (1995) Tertiäre Vegetationgeschichte Europas. Gustav Fischer, Jena Stuttgart, New York

    Google Scholar 

  • Martín JL, Arechavaleta M, Borges PAV, Faria B (eds) (2008a) As cem espécies ameaçadas prioritárias em termos de gestão na região europeia biogeográfica da Macaronésia. Consejería de Medio Ambiente y Ordenación Territorial, Gobierno de Canarias

    Google Scholar 

  • Martín JL, Arechavaleta M, Borges PAV, Faria B (2008b) A perspectiva macaronésia. In: Martín JLA, Arechavaleta M, Borges PAV, Faria B (eds) TOP 100—as cem espécies ameaçadas prioritárias em termos de gestão na região europeia biogeográfica da Macaronésia. Consejería de Medio Ambiente y Ordenación Territorial, Gobierno de Canarias, pp 389–420

    Google Scholar 

  • Martins FEO (1981) Mobiliário Açoriano, elementos para o seu estudo. Direcção Regional dos Assuntos Culturais, Angra do Heroísmo

    Google Scholar 

  • Martins AMF (1993) The Azores—Westernmost Europe: where evolution can be caught red-handed. Bol Mus Mun Funchal Sup N 2:181–198

    Google Scholar 

  • Médail F, Quézel P (1997) Hot-spots analysis for conservation of plant biodiversity in the Mediterranean Basin. Annals Missouri Bot Gard 84:112–127

    Article  Google Scholar 

  • MedCalc S (2009) Digimizer 3.6.0. Gent, Belgium

    Google Scholar 

  • Mitchell AK (1998) Acclimation of Pacific yew (Taxus brevifolia) foliage to sun and shade. Tree Physiol 18:749–757. doi:10.1093/treephys/18.11.749

    PubMed  Google Scholar 

  • Morandini R, Ducci F, Menguzzato G (1994) Abies nebrodensis (Lojac.) Mattei. Inventario1992. Ann Ist Sper Selv XXII:5–51

    Google Scholar 

  • Parducci L, Szmidt AE, Madaghiele A, Anzidei M, Vendramin GG (2001) Genetic variation at chloroplast microsatellites (cpSSRs) in Abies nebrodensis (Lojac.) Mattei and three neighboring Abies species. Theor Appl Genet 102:733–740. doi:10.1007/s001220051704

    Article  CAS  Google Scholar 

  • Pereira MJ, Arruda R, Furtado D, Cabral N (2007) Breve caracterização da flora vascular corvina. XIII Expedição Científica do Departamento de Biologia—Flores e Corvo 2007, Rel Com Dep Biol 35:123. Universidade dos Açores, Ponta Delgada

    Google Scholar 

  • Pinheiro J (2007) Génese e características dos Andossolos dos Açores. Angra do Heroísmo, Universidade dos Açores, Associate, Portugal

    Google Scholar 

  • Piovesan G, Presutti Saba E, Biondi F, Alessandrini A, Di Filippo A, Schirone B (2009) Population ecology of yew (Taxus baccata L.) in the Central Apennines: spatial patterns and their relevance for consrvation strategies. Plant Ecol (in press) doi:10.1007/s11258-009-9596-1

  • Royal Botanic Gardens, Kew (2003) http://www.kew.org/. Cited on 5 Aug 2009

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497. doi:10.1093/bioinformatics/btg359

    Article  CAS  PubMed  Google Scholar 

  • Salisbury EJ (1927) On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Philos Trans R Soc London B216:1–65

    Google Scholar 

  • Schafer H (2002) Flora of the Azores. A Fieldguide. Margraf-Verlag, Weikersheim

    Google Scholar 

  • Seubert M, Hochstetter C (1843) Übersicht der Flora der azorischen Inseln. Archiv für Naturgeschichte 9:1–24

    Google Scholar 

  • Spada F (2003) Considerazioni sulla fitogeografia e sulla genesi delle comunità a Taxus baccata L. in Europa. In: Schirone B, Bellarosa R, Piovesan G (eds) Il Tasso—un albero da conoscere e conservare. Cogecstre Edizioni, Viterbo, pp 13–33

    Google Scholar 

  • Spjut RW (2007a) A phytogeographical analysis of Taxus (Taxaceae) based on leaf anatomical characters. J Bot Res Inst Texas 1(1):291–332

    Google Scholar 

  • Spjut RW (2007b) Taxus baccata alliance. http://www.worldbotanical.com/index.html#outline

  • Spjut RW (2008) Introduction to Taxus: methodology, taxonomic relationships, leaf and seed characters, phytogeographical relationships, cultivation, and chemistry. Section on nomenclatural problems. http://www.worldbotanical.com/index.html#outline

  • SRAM (2005) Plano Sectorial para a Rede Natura 2000 para a Região Autónoma dos Açores. Horta, Secretaria Regional do Ambiente e do Mar (SRAM)

  • Strobel GA, Hess WM, Ford E (1996) A scanning electron microscopy study of Taxus leaves as related to taxonomy. Scanning Microsc 10(4):1111–1126

    CAS  PubMed  Google Scholar 

  • Sunding P (1979) Origins of the Macaronesian flora. In: Bramwell D (ed) Plants and Islands. London, pp 13–40

  • Svenning JC, Magård E (1999) Population ecology and conservation status of the last natural population of English yew Taxus baccata in Denmark. Biol Conserv 88:173–182. doi:10.1016/S0006-3207(98)00106-2

    Article  Google Scholar 

  • Sweeney CA (2004) A key for the identification of stomata of the native conifers of Scandinavia. Rev Palaeobot Palynol 128(2004):281–290. doi:10.1016/S0034-6667(03)00138-6

    Article  Google Scholar 

  • Takhtajan A (1969) Flowering plants: origin and dispersal. Oliver & Boyd, Edinburgh

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092

    Article  CAS  PubMed  Google Scholar 

  • Thomas PA, Polwart A (2003) Biological flora of the British Isles—Taxus baccata L. J Ecol 91:489–524

    Article  Google Scholar 

  • Thompson JD, Higgins DJ, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Trelease W (1897) Botanical Observations on the Azores. In: Missouri botanical garden (edn): Missouri botanical garden eight annual report. Missouri Botanical Garden, St. Louis, pp 77–220

  • Tutin TG (1953) The vegetation of the Azores. J Ecol 41(1):53–61

    Article  Google Scholar 

  • Tutin TG, Heywood VH, Burges NA, Valentine DH, Walters SM, Webb DA (1972) Flora Europeae—Lycopodiaceae to Plataneaceae. Cambridge University Press, Cambridge

    Google Scholar 

  • Van Riel P, Jordaens K, Van Houtte N, Martins AMF, Verhagen R, Backeljau T (2005) Molecular systematics of the endemic Leptaxini (Gastropoda: Pulmonata) on the Azores islands. Mol Phylogenet Evol 37:132–143. doi:10.1016/j.ympev.2005.03.019

    Article  PubMed  Google Scholar 

  • Vargas P (2007) Are Macaronesian islands refugia of relict plant lineages?: a molecular survey. In: Weiss S, Ferrand N (eds) Phylogeography of Southern European Refugia. Springer, Berlin, Heidelberg, New York, pp 297–314

    Chapter  Google Scholar 

  • Vaxevanidou Z, González-Martínez SG, Climent J, Gil L (2006) Tree populations bordering on extinction: a case study in the endemic Canary Island pine. Biol Conserv 129:451–460. doi:10.1016/j.biocon.2005.11.012

    Article  Google Scholar 

  • Watson HC (1870) Botany of the Azores. Natural history of the Azores or Western Islands. Godman FDC, London

    Google Scholar 

  • Webster JW (1821) Description of the Island of St. Michael. RP & C Williams, Boston

    Google Scholar 

  • Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography—ecology, evolution and conservation. London OUP, London

  • Willmer CM, Fricker M (1996) Stomata. Chapman & Hall, London

    Google Scholar 

  • World Conservation Monitoring Centre (1998) Ramosmania rodriguesii. In: IUCN 2009. IUCN red list of threatened species, Version 2009.1. www.iucnredlist.org. Retrieved 5 Aug 2009

Download references

Acknowledgments

We are indebted to Dr Ana Paula Marques, the former Environment and Sea Regional Secretary of Azores, for conceding a grant and for the logistic support her department provide and to MSc Benilde Pereira for her valuable help and committement on the field work performed in Pico Island. Special thanks to Dr Roberta Piredda for the bioinformatics support.

Author information

Authors and Affiliations

  1. Dipartimento Di tecnologie, ingegneria e scienze dell’Ambiente e delle Foreste (DAF), Facoltà di Agraria, Università della Tuscia, Via San Camillo de’ Lellis, snc, 01100, Viterbo, Italy

    Bartolomeo Schirone, Raquel Caetano Ferreira, Federico Vessella, Avra Schirone, Roberta Piredda & Marco Cosimo Simeone

Authors
  1. Bartolomeo Schirone
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Raquel Caetano Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Federico Vessella
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Avra Schirone
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roberta Piredda
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marco Cosimo Simeone
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bartolomeo Schirone.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schirone, B., Ferreira, R.C., Vessella, F. et al. Taxus baccata in the Azores: a relict form at risk of imminent extinction. Biodivers Conserv 19, 1547–1565 (2010). https://doi.org/10.1007/s10531-010-9786-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-010-9786-0

Keywords

Search

Navigation