Skip to main content

Advertisement

Log in

Do secondary sexual dimorphism and female intolerance to drought influence the sex ratio and extinction risk of Taxus baccata?

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

Sex ratio and sexual dimorphism were studied in the dioecious tree Taxus baccata. We examined five populations of T. baccata in Poland and Ukraine to identify the differences between male and female individuals. The sex of all individuals, height and diameter, needle length and area, specific leaf area (SLA), the number of stomata rows, stomatal density, and content of carbon and nitrogen were measured to identify the differences between male and female individuals. The relationship between sex ratio and climatic conditions, age and population size were analysed using data collected from the field and the literature. Female trees were shorter than males, but needles of females were longer and had larger area. Although there were no differences among sexes in SLA, nitrogen and carbon concentration, we found a positive correlation between nitrogen concentration and SLA among females. The sex ratio changed with tree height within populations, and taller height classes were biased in favour of males. Regardless of population age, the percentage of females within populations was positively correlated with precipitation. Probably high reproductive effort caused female trees to lose in competition with males, and this loss may also be enhanced by lower drought tolerance in females and could contribute to risk of extinction for T. baccata. The continental geographic range of T. baccata may be restricted by limited occurrence of females, which demand higher water resources than males.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Baldoni M, Biondi E, Ferrante L (2004) Demographic and spatial analysis of a population of Juniperus oxycedrus L. in an abandoned grassland. Plant Biosyst 138:89–100. doi:10.1080/11263500412331283735

    Article  Google Scholar 

  • Bañuelos MJ, Obeso JR (2004) Resource allocation in the dioecious shrub Rhamnus alpinus. Evol Ecol Res 6:397–413

    Google Scholar 

  • Bertiller MB, Sain CL, Carrera AL (2002) Effect of fine-scale spatial variation of soil nitrogen on the performance of the sexes of Poa ligularis in patchy ecosystems of northern Patagonia. Int J Plant Sci 163(3):419–425. doi:10.1086/339515

    Article  Google Scholar 

  • Bodziarczyk J, Zator A (2004) Rozmieszczenie, struktura i warunki występowania populacji cisa pospolitego Taxus baccata L. w paśmie Łysej Góry w Beskidzie Niskim. Acta Agraria Silvestria 43:3–20

    Google Scholar 

  • Boratyński A, Kmiecik M, Koniński P, Kwiatkowski P, Szczęśniak E (1997) Chronione i godne ochrony drzewa i krzewy polskiej części Sudetów, Pogórza i Przedgórza Sudeckiego. 9. Taxus L. Arboretum Kornickie 42:111–147

  • Browicz K, Gostyńska-Jakuszewska M (1969) Taxus L. In: Białobok W, Browicz K (eds) Atlas rozmieszczenia drzew i krzewów w Polsce. PWN, Warszawa-Poznań, pp 5–14

    Google Scholar 

  • Chomicz K, Samej F (1974) Stosunki opadowe. In: Koncek M (ed) Klima Tatier. Vyd Slov Akad Vied, Bratislava, Slovakia, pp 443–536

    Google Scholar 

  • Cipollini ML, Stiles EW (1991) Costs of reproduction in Nyssa sylvatica: sexual dimorphism in reproductive frequency and nutrient flux. Oecologia 86:585–593. doi:10.1007/BF00318326

    Article  Google Scholar 

  • Cipollini ML, Whigham DF (1994) Sexual dimorphism and cost of reproduction in the dioecious shrub Lindera benzoin (Lauraceae). Am J Bot 81:65–75. doi:10.2307/2445564

    Article  Google Scholar 

  • Dawson TE, Ehleringer JR (1993) Gender-specific physiology, carbon isotope discrimination, and habitat distribution in boxelder, Acer negundo. Ecology 74:798–815. doi:10.2307/1940807

    Article  Google Scholar 

  • Dudley LS (2006) Ecological correlates of secondary sexual dimorphism in Salix glauca (Salicaceae). Am J Bot 93:1775–1783. doi:10.3732/ajb.93.12.1775

    Article  Google Scholar 

  • Dudley LS, Galen C (2007) Stage-dependent patterns of drought tolerance and gas exchange vary between sexes in the alpine willow, Salix glauca. Oecologia 153(1):1–9. doi:10.1007/s00442-007-0712-4

    Article  PubMed  Google Scholar 

  • Ellenberg H, Weber HE, Düll R, Wirth V, Werner W, Paulißen D (1991) Zeigerwerte von Pflanzen in Mitteleuropa. Scr Geobotanica 18:3–248

    Google Scholar 

  • Eppley SM (2001) Gender-specific selection during early life-history stages in the dioecious grass Distichlis spicata. Ecology 82:2022–2031

    Google Scholar 

  • Espirito-Santo MM, Madeira BG, Neves FS, Faria ML, Fagundes M, Fernandes GW (2003) Sexual differences in reproductive phenology and their consequences for the demography of Baccharis dracunculifolia (Asteraceae), a dioecious tropical shrub. Ann Bot (Lond) 91:13–19. doi:10.1093/aob/mcg001

    Article  CAS  Google Scholar 

  • Faliński JB (1998) Dioecious woody pioneer species (Juniperus communis, Populus tremula, Salix s-p. div.) in the secondary succession and regeneration. Phytocoenosis 8 (N.S.) Seminarium Geobotanicum 10

  • Freeman DC, Klikoff LG, Harper KT (1976) Differential resource utilization by the sexes of dioecious plants. Science 193:597–599. doi:10.1126/science.193.4253.597

    Article  PubMed  Google Scholar 

  • Garcia D, Zamora R, Hodar JA (2000) Yew (Taxus baccata L.) regeneration is facilitated by fleshy-fruited shrubs in Mediterranean environments. Biol Conserv 95:31–38. doi:10.1016/S0006-3207(00)00016-1

    Article  Google Scholar 

  • Giertych P (2000) Factors determining natural regeneration of yew (Taxus baccata L.) in the Kórnik Arboretum. Dendrobiology 45:31–40

    Google Scholar 

  • Givnish TJ (1980) Ecological constraints on the evolution of breeding systems in seed plants: dioecy and dispersal in gymnosperms. Evol Int J Org Evol 34:959–972. doi:10.2307/2408001

    Google Scholar 

  • Głowacka M, Michalski G, Gancarczyk-Gola M (2004) Populacja cisa pospolitego (Taxus baccata L.) w rezerwacie „Cisy w Hucie Starej” w województwie śląskim. Parki Narodowe i Rezerwaty Przyrody 23:541–553

    Google Scholar 

  • Grill D, Tausz M, Pollinger U, Jimenez MS, Morales D (2004) Effects of drought on needle anatomy of Pinus canariensis. Flora 199:85–89

    Google Scholar 

  • Heilbuth JC (2000) Lower species richness in dioecious clades. Am Nat 156:221–241. doi:10.1086/303389

    Article  Google Scholar 

  • Heilbuth JC, Illves K, Otto SP (2001) The consequences of dioecy for seed dispersal: modeling the seed-shadow handicap. Evol Int J Org Evol 55:880–888. doi:10.1554/0014-3820(2001)055[0880:TCODFS]2.0.CO;2

    CAS  Google Scholar 

  • Hilfiker K, Gugerli F, Schutz JP, Rotach P, Holderegger R (2004) Low RAPD variation and female-biased sex ratio indicate genetic drift in small populations of the dioecious conifer Taxus baccata in Switzerland. Conserv Genet 5:357–365. doi:10.1023/B:COGE.0000031144.95293.1b

    Article  CAS  Google Scholar 

  • Holtmeier FK (2003) Mountain timberlines. Ecology, patchiness, and dynamics. Kluwer Academic Publishers, Dordrecht, Boston, London

    Google Scholar 

  • Hulme P (1996) Natural regeneration of yew (Taxus baccata L.), microsite, seed or herbivore limitation? J Ecol 84:853–861. doi:10.2307/2960557

    Article  Google Scholar 

  • Hultine KR, Bush SE, West AG, Ehleringer JR (2007) Population structure, physiology and ecohydrological impacts of dioecious riparian tree species of western North America. Oecologia 154(1):85–93

    Article  PubMed  CAS  Google Scholar 

  • Iglesias MC, Bell G (1989) The small-scale spatial distribution of male and female plants. Oecologia 80:229–235

    Google Scholar 

  • Iszkuło G (2001) The yew (Taxus baccata L.) of the Cisowy Jar reserve near Olecko. Dendrobiology 46:33–37

    Google Scholar 

  • Iszkuło G, Boratyński A (2004) Interaction between canopy tree species and European yew Taxus baccata (Taxaceae). Pol J Ecol 52:523–531

    Google Scholar 

  • Iszkuło G, Boratyński A (2005) Different age and spatial structure of two spontaneous subpopulations of Taxus baccata as a result of various intensity of colonization process. Flora 200:195–206

    Google Scholar 

  • Iszkuło G, Boratyński A (2006) Analysis of the relationship between photosynthetic photon flux density and natural Taxus baccata seedlings occurrence. Acta Oecol 29:78–84. doi:10.1016/j.actao.2005.08.001

    Article  Google Scholar 

  • Iszkuło G, Jasińska AK (2004) Variation in sex expression in Polish and Ukrainian populations of Taxus baccata L. Dendrobiology 52:29–32

    Google Scholar 

  • Jalas J, Suominen J (1973) Atlas Florae Europea. Distribution of vascular plants in Europe. 2. Gymnospermae, Helsinki

    Google Scholar 

  • Jong TJ, Meijden E (2004) Sex ratio of some long-lived dioecious plants in a sand dune area. Plant Biol 6:616–620. doi:10.1055/s-2004-821177

    Article  PubMed  Google Scholar 

  • Koncek M, Orlicz M (1974) Stosunki termiczne. In: Koncek M (ed) Klima Tatier. Vyd. Slov. Akad. Vied, Bratislava, pp 89–180

    Google Scholar 

  • Krischik VA, Denno RF (1990) Patterns of growth, reproduction, defense, and herbivory in the dioecious shrub Baccharis halimifolia (Compositae). Oecologia 83:182–190. doi:10.1007/BF00317750

    Article  Google Scholar 

  • Krishnan RM, Ramesh BR (2005) Endemism and sexual systems in the evergreen tree flora of the Western Ghats, India. Divers Distrib 11:559–565. doi:10.1111/j.1366-9516.2005.00190.x

    Article  Google Scholar 

  • Król S (1986) Struktura i rozwój różnowiekowej populacji Taxus baccata L. naturalnego pochodzenia w północno-zachodniej Polsce. Acta Universitatis Lodzensis. Folia Sozologica 3:173–191

    Google Scholar 

  • Laporte MM, Delph LF (1996) Sex-specific physiology and source-sinkrelations in the dioecious plant Silene latifolia. Oecologia 106:63–72

    Google Scholar 

  • Leigh A, Cosgrove MJ, Nicotra AB (2006) Reproductive allocation in a gender dimorphic shrub: anomalous female investment in Gynatrix pulchella? J Ecol 94:1261–1271. doi:10.1111/j.1365-2745.2006.01164.x

    Article  Google Scholar 

  • Li C, Yang Y, Junttila O, Palva T (2005) Sexual differences in cold acclimation and freezing tolerance development in sea buckthorn (Hippophae rhamnoides L.) ecotypes. Plant Sci 168:1365–1370. doi:10.1016/j.plantsci.2005.02.001

    Article  CAS  Google Scholar 

  • Li C, Xu G, Zang R, Korpelainen H, Berninger F (2007) Sex-related differences in leaf morphological and physiological responses in Hippophae rhamnoides along an altitudinal gradient. Tree Physiol 27:399–406

    PubMed  CAS  Google Scholar 

  • Lloyd DG, Webb CJ (1977) Secondary sex characters in plants. Bot Rev 43:177–216. doi:10.1007/BF02860717

    Article  Google Scholar 

  • Massei G, Watkins R, Hartley SE (2006) Sex-related growth and secondary compounds in Juniperus oxycedrus macrocarpa. Acta Oecol 29:135–140. doi:10.1016/j.actao.2005.08.004

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Montesinos D, De Luis M, Verdu M, Raventos J, Garcia-Fayos P (2006) When, how and how much: gender-specific resource-use strategies in the dioecious tree Juniperus thurifera. Ann Bot (Lond) 98:885–889. doi:10.1093/aob/mcl172

    Article  CAS  Google Scholar 

  • Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348. doi:10.1046/j.1469-8137.2002.00477.x

    Article  Google Scholar 

  • Obeso JR, Alvarez-Santullano M, Retuerto R (1998) Sex ratios, size distributions, and sexual dimorphism in the dioecious tree Ilex aquifolium (Aquifoliaceae). Am J Bot 85:1602–1608. doi:10.2307/2446488

    Article  Google Scholar 

  • Orębska-Stralkowa B (1983) Stosunki klimatyczne w rejonie Babiej Góry In: Zabierowski K (ed) Park Narodowy na Babiej Górze. Człowiek i przyroda. Studia Naturae, B PWN, Warszawa, Kraków, pp 41–62.

  • Ortiz PL, Arista M, Talavera S (1998) Low reproductive success in two subspecies of Juniperus oxycedrus L. Int J Plant Sci 159:843–847. doi:10.1086/297605

    Article  Google Scholar 

  • Palacio S, Milla R, Montserrat-Marti G (2005) A phenological hypothesis on the thermophilous distribution of Pistacia lentiscus L. Flora 200:527–534

    Google Scholar 

  • Pannell JR, Barrett SCH (1998) Baker’s Law revisited: reproductive assurance in a metapopulation. Evol Int J Org Evol 52:657–668. doi:10.2307/2411261

    Google Scholar 

  • Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC et al (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969

    Article  Google Scholar 

  • Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606. doi:10.2307/2445418

    Article  Google Scholar 

  • Rottenberg A (1998) Sex ratio and gender stability in the dioecious plants of Israel. Bot J Linn Soc 128:137–148

    Article  Google Scholar 

  • Sawyer NW, Anderson GJ (1998) Reproductive biology of the carrion-flower, Smilax herbacea (Smilacaceae). Rhodora 100:1–24

    Google Scholar 

  • 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 

  • Thomas PA, Polwart A (2003) Taxus baccata L. biological flora of the British Isles 229. J Ecol 91:489–524. doi:10.1046/j.1365-2745.2003.00783.x

    Article  Google Scholar 

  • Tumiłowicz J (1965) Wzrost i pielęgnowanie cisów (Taxus baccata L.) w arboretum w Rogowie. Sylwan 109:47–53

    Google Scholar 

  • Vamosi JC, Vamosi SM (2005) Present day risk of extinction may exacerbate the lower species richness of dioecious clades. Divers Distrib 11:25–32. doi:10.1111/j.1366-9516.2005.00119.x

    Article  Google Scholar 

  • Ward JK, Dawson TE, Ehleringer JR (2002) Responses of Acer negundo genders to interannual differences in water availability determined from carbon isotope ratios of tree ring cellulose. Tree Physiol 22:339–346

    PubMed  CAS  Google Scholar 

  • Wheelwright NT, Logan BA (2004) Previous-year reproduction reduces photosynthetic capacity and slows lifetime growth in females of a neotropical tree. Proc Natl Acad Sci USA 101:8051–8055. doi:10.1073/pnas.0402735101

    Article  PubMed  CAS  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle

    Google Scholar 

  • Zarzycki K, Trzcińska-Tacik H, Różański W, Szeląg Z, Wołek J, Korzeniak U (2002) Ecological indicator values of vascular plants of Poland. Biodivers Pol 2:5–183

    Google Scholar 

  • Zunzunegui M, Diaz Barradas MC, Clavijo A, Cansino LA, Lhout FA, Novo FG (2006) Ecophysiology, growth timing and reproductive effort of three sexual forms of Corema album (Empetraceae). Plant Ecol 183:35–46. doi:10.1007/s11258-005-9004-4

    Article  Google Scholar 

Download references

Acknowledgements

The investigations were partly supported by Polish Committee for Scientific Research Grant No. 2 P60L 023 26. The authors thank Jacek Oleksyn for helpful comments that significantly improved the manuscript. We are grateful to Dr. Lee E. Frelich for language correction of final version of the manuscript. We also thank Mirka Piórkowska, Ola, Piotr, Bogdan Jasiński and Iza, Ola, Kuba, Oksana, Marek Kmiecik for help in the field and logistical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Grzegorz Iszkuło.

Appendix 1

Appendix 1

Population

Geographical position

Altitude (m)

Number of individuals in population

Sex ratio (% females)

Source

Denmark, Munkebjerg

N 55° 41′ E 9° 37′

44

2,000

67

Svenning and Magård (1999)

Poland, Czarne

N 53° 41′ E 16° 56′

135

428

47

Fałtynowicz and Markowski (unpublished data)

Poland, Rogów Arboretum

N 51° 49′ E 19° 52′

150

380

38

Tumiłowicz (1965)

Poland, Pommerania, Wierzchlas

N 53° 52′ E 18° 07′

105

3,500

33

Authors

Poland, Kórnik Arboretum

N 52° 25′ E 17° 06′

70

3,000

48

Authors

Poland, Huta Stara

E 50° 32′ E 19° 15′

350

51

41

Głowacka et al. (2004)

Poland, Sudety Mts., Cisy

N 50° 50′ E 16° 30′

410

1,035

46

Authors

Poland, Sudety Mts., Cisowa Góra

N 50° 50′ E 16° 30′

450

757

47

Authors

Poland, Wąwoz Myśliborski

N 51° 01′ E 16° 07′

340

73

39

Boratyński et al. (1997)

Poland, Sudety Mts. Nowy Waliszów

N 50° 18′ E 16° 44′

600

697

46

Boratyński et al. (1997)

Poland, Sudety Mts., Książ

N 50° 50′ E 16° 18′

400

300

24

Boratyński et al. (1997)

Poland, Carpathians, Dukla

N 49° 34′ E 21° 34′

550

1,585

48

Bodziarczyk and Zator (2004)

Ukraine, Carpathians, Kniazhdvir

N 48° 50′ E 24° 50′

400

15,000

46

Authors

Switzerland, Vorberg, Rüttenen

N 47° 13′ E 7° 31′

860

650

54

Hilfiker et al. (2004)

Switzerland, Dottenberg, Lostorf

N 47° 23′ E 7° 56′

870

700

55

Hilfiker et al. (2004)

Switzerland, Einolte, Oberhof

N 47° 26′ E 8° 01′

700

60

62

Hilfiker et al. (2004)

Switzerland, Uetliberg–Falätschen, Zürich

N 47° 22′ E 8° 32′

750

2,500

52

Hilfiker et al. (2004)

Switzerland, Scheren–Sihl, Schindellegi

N 47° 10′ E 8° 42′

800

300

56

Hilfiker et al. (2004)

Switzerland, Etzelwald, Feusisberg

N 47° 11′ E 8° 46′

810

47

68

Hilfiker et al. (2004)

Switzerland, Guegenhard, Elgg

N 47° 29′ E 8° 51′

570

1,600

50

Hilfiker et al. (2004)

Switzerland, Schneitberg–Affenberg, Elgg

N 47° 31′ E 8° 53′

650

68

60

Hilfiker et al. (2004)

Switzerland, Hagebuechtobel, Zuzwil–Wuppenau

N 47° 29′ E 9° 06′

610

550

55

Hilfiker et al. (2004)

Switzerland, Schoostobel, Oberbüren–Niederbüren

N 47° 24′ E 09° 13′

560

150

49

Hilfiker et al. (2004)

Switzerland, Unterer Darewald, Salgesch

N 46° 18′ E 7° 34′

1,080

500

55

Hilfiker et al. (2004)

Switzerland, Blindtal, Naters

N 46° 21′ E 8° 01′

1,200

35

51

Hilfiker et al. (2004)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Iszkuło, G., Jasińska, A.K., Giertych, M.J. et al. Do secondary sexual dimorphism and female intolerance to drought influence the sex ratio and extinction risk of Taxus baccata?. Plant Ecol 200, 229–240 (2009). https://doi.org/10.1007/s11258-008-9447-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-008-9447-5

Keywords

Navigation