C.R. Acad. Sci.

Paris, Sciences de la vie / Life Sciences 324 (2001) 245–250

© 2001 Académie des sciences/Éditions scientifiques et médicales Elsevier SAS. Tous droits réservés
S0764446900012890/FLA

Plant biology and pathology / Biologie et pathologie végétale

Dioecy in Fitzroya cupressoides (Molina) I.M.

Johnst. and Pilgerodendron uviferum (D. Don.)
Florin (Cupressaceae)
Javier Grosfelda,b, Daniel Barthélémyb*
a
Centro Reg. Univ. Bariloche, Univ. Nac. del Comahue, Concejo Nacional de Investigaciones Científicas y
Técnicas (CONICET), 8400 Bariloche, Argentina
b
Unité mixte de recherche Cirad/Inra, Modélisation des plantes (Amap), TA40/E, 34398 Montpellier cedex 5,
France
Received 7 August 2000; accepted 30 October 2000
Communicated by Michel Thellier

Abstract – The aim of this study was to determine the dioecious or monoecious
condition of Fitzroya cupressoides and Pilgerodendron uviferum. The study area lies
west of the Nahuel Huapi National Park in northern Patagonia (Argentina), where these
species form mixed stands. One hundred individuals of each species were studied over
three successive years. The nature and position in the crown of their reproductive organs
were recorded. Results showed that both species are dioecious. This feature has been
confirmed on trees of these species growing in other sites within their natural distribution
area in Argentina and Chile. © 2001 Académie des sciences/Éditions scientifiques et
médicales Elsevier SAS

Dioecy / Fitzroya cupressoides / Pilgerodendron uviferum / Cupressaceae / Patagonia

Résumé – Dioécie chez Fitzroya cupressoides (Molina) I.M. Johnst. et Pilgero-

dendron uviferum (D. Don.) Florin (Cupressaceae). En regard des controverses
bibliographiques au sujet de l’état dioïque ou monoïque de Fitzroya cupressoides et
Pilgerodendron uviferum, l’objectif de ce travail est de déterminer la distribution des
organes reproducteurs chez ces deux espèces. L’étude se situe à l’ouest du parc national
nahuel Huapi au nord-ouest de la Patagonie (Argentine). Pendant trois années et pour
chaque espèce, cent individus ont été suivis en notant la nature et la position des
organes reproducteurs dans la cime des arbres. Les résultats de cette étude montrent que
ces deux espèces sont dioïques. Cette caractéristique a été confirmée sur de nombreux
individus en Argentine et au Chili. © 2001 Académie des sciences/Éditions scientifiques
et médicales Elsevier SAS
Dioécie / Fitzroya cupressoides / Pilgerodendron uviferum / Cupressaceae / Patagonie

Version abrégée
Fitzroya cupressoides se trouve, à l’état naturel, en
Argentine et au Chili entre 39° 50’ et 43° 30’ de latitude
sud. Ces arbres peuvent atteindre une hauteur de plus
de 50 m et un diamètre de 4 m. Certains individus de
cette espèce figurent parmi les arbres les plus âgés du
monde et peuvent dépasser 3 600 ans. Pilgerodendron
uviferum est également une espèce endémique des
forêts subantarctiques d’Amérique du Sud. Son aire de
répartition se situant entre 39° 30’et 55° 30’ de latitude
sud, cette espèce est la plus australe des conifères.

* Correspondence and reprints.

E-mail address: barthelemy@cirad.fr (D. Barthélémy).

245
 J. Grosfeld, D. Barthélémy / C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 245–250
Surexploitées ces derniers siècles, ces deux espèces
sont maintenant protégées par des lois nationales et
des conventions internationales. Comme chez les autres
coniférales, les cônes sont unisexués, mais les informa-
tions bibliographiques sont contradictoires en ce qui
concerne la condition monoïque ou dioïque des deux
espèces. Le but de cette étude est de déterminer la
distribution des cônes sur les individus en forêts natu-
relles.
Nous avons sélectionné une parcelle de 3 ha située à
l’ouest du parc national Nahuel Huapi (Argentine).
Cent individus de chaque espèce ont été marqués et
suivis pendant trois années consécutives. Pour chaque
individu, nous avons noté la nature et la position des
organes reproducteurs dans la couronne des arbres. La
cime de chaque individu a été examinée dans sa
totalité. D’autre part, plusieurs centaines d’arbres de
ces deux espèces ont été examinés ponctuellement en
forêts naturelles et en divers points de leur aire de
répartition en Argentine et au Chili.
Les organes reproducteurs se situent toujours en
position terminale sur les rameaux d’ordre ultime. Sauf
pour un individu de F. cupressoides, les cônes mâles et
femelles sont toujours portés par des individus diffé-
rents et les deux espèces sont donc dioïques. On peut
écarter l’hypothèse que les deux espèces sont dioïques
1. Introduction
The ‘Alerce’, Fitzroya cupressoides (Molina) I.M. Johnst.,
is a giant conifer tree, endemic to southern Chile and
Argentina where it grows naturally as discontinuous popu-
lations between 39° 50’ and 43° 30’ lat. S., from the
Cordillera de la Costa range, south of Valdivia, to the
Andes [1]. It generally occurs at elevations from 100 to
1 200 m in humid areas on poorly drained or waterlogged,
nutrient-poor or incipient volcanic soils. Reaching a height
of over 50 m and with a stem diameter greater than 4 m [2,
3], Fitzroya cupressoides is the second oldest living tree
species of the world, with a cross-dated age of 3 622 years
[4].
The ‘Ciprés de las Guaytecas’, Pilgerodendron uviferum
(D. Don.) Florin, occurs in Chile and Argentina from 39°
30’ to 55° 30’ lat. S. and represents the southernmost
conifer in the world [3, 5]. This species often grows in
association with Fitzroya in its northern distribution area;
it is most characteristically found in poorly drained areas
at low to mid elevations in the Andes and in humid coastal
forests [6]. Whilst not as long living as Fitzroya, it can live
up to 500 years [7].
Because of the beauty and high quality of their wood,
these two species were intensively harvested in past cen-
turies [1, 3, 8]. They are now fully protected by national
laws and under Appendix I of CITES (Convention on
International Trade in Endangered Species) [6, 8, 9].
246
seulement pendant une étape de leur développement,
vu que l’âge des arbres étudiés est très varié.
Les controverses de la littérature au sujet de l’état
dioïque ou monoïque des deux espèces peuvent être
attribuées aux raisons suivants : 1) l’usage équivoque
des termes dioïque ou monoïque pour les « fleurs » ou
cônes, alors que ces termes devraient se référer à la
distribution des organes reproducteurs sur les indivi-
dus d’une même espèce, 2) l’observation antérieure
d’un matériel végétal étudié hors de son aire d’origine
naturelle ou dont l’origine n’est parfois pas précisée ou
encore l’étude d’individus au comportement excep-
tionnel pour l’espèce, 3) la citation successive de
références bibliographiques sans une confirmation
directe des observations ou sans nouvelles collectes de
matériel végétal.
Les arbres observés ayant été analysés en divers
points de l’aire de répartition naturelle de ces deux
espèces, il semble logique de penser que la dioécie
représente une caractéristique de tous les individus de
chaque espèce étudiée. Une meilleure connaissance de
l’expression de la sexualité chez ces deux espèces est
importante pour leur gestion ainsi que pour la compré-
hension des relations phylogénétiques chez les Cupres-
saceae d’Amérique du Sud et plus généralement entre
les espèces de l’hémisphère Sud.
Together with Austrocedrus chilensis (D. Don.) Florin,
these two species are the only endemic Cupressaceae of
the sub-Antarctic and Patagonian forests of South America
[6]. As with other Coniferales, in all normal circumstances,
each of these species develops two distinct types of stro-
bili, i.e. microsporangiate or pollen-bearing cones and
megasporangiate or seed cones [10]. However for these
Patagonian Cupressaceae contradictory reports exist con-
cerning their monoecious or dioecious condition. Brion et
al. [11] and Castor et al. [12] recently demonstrated that
Austrocedrus chilensis is a dioecious species. Neverthe-
less, despite its importance for the management and con-
servation of these protected species, monoecious or dioe-
cious condition in Fitzroya cupressoides and
Pilgerodendron uviferum is still unclear as reported in
published data.
Moore [5], Dallimore and Jackson [13], Den Ouden and
Boom [14], Hoffman [15], Dimitri et al. [16] and Brion
[17] indicate that Pilgerodendron uviferum is a monoe-
cious tree, but Covas [18] affirms that it is dioecious.
However, Barret [19] describes it as a tree with ‘monoe-
cious or dioecious flowers’ whereas Muñoz Shick [20] and
Marticorena and Rodriguez [21] point out that its flowers
are dioecious.
According to Elwes and Henry ([22] in [23]), Dallimore
and Jackson [13], Pardé [24] and Gaussen [25], Fitzroya
cupressoides has ‘male and female flowers’ on the same or
on different trees and sometimes ‘flowers’ are hermaphro-
 J. Grosfeld, D. Barthélémy / C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 245–250
Figure 1. Map showing the location of the sample site (Puerto Blest, shaded area).
dite. Den Ouden and Boom [14], Dimitri et al. [16], Covas
[18], Barret [19], Tortorelli [26], Callen [27], Rodriguez et
al. [28], and Welch [29] consider this species as dioecious
or monoecious. Hoffman [15] and Marticorena and Rod-
riguez [21] speak of ‘dioecious flowers’.
For both species, observations on their reproductive
phenology in Chilean forests revealed that seed produc-
tion is annually very variable [3, 30, 31], but none of these
studies reports on the expression of sexuality in natural
populations.
The objective of the present work was to study system-
atically the distribution of the reproductive organs (i.e. the
monoecious or dioecious condition) of F. cupressoides
and P. uviferum trees in natural forest condition in north-
ern Patagonia (Argentina).
2. Materials and methods
A 3-ha mixed stand of F. cupressoides and P. uviferum
trees was selected in the Puerto Blest area of the Nahuel
Huapi National Park (Argentina), at 41° 04’S and 71°
46’W (figure 1). With an annual mean precipitation of
approximately 3 500 mm/year at an elevation of approxi-
mately 760 m [17] and poorly drained soils, this site is
representative of the general conditions in which both
species normally grow in their natural area of distribution.
For both species, 100 adult individuals were selected at
random. The diameter at breast height (d.b.h.) of all
selected trees was recorded (P. uviferum: d.b.h. max. =
38.2 cm, d.b.h. min. = 3.1 cm, mean ± standard deviation
= 12.3 ± 4.2; F. cupressoides: d.b.h. max. = 62.0 cm, d.b.h.
min. = 3.7 cm, mean ± standard deviation = 15.5 ± 6.8).
The types and positions of reproductive organs within the
crown were recorded for each individual. Each specimen
was examined with binoculars in its totality from the
lowest to the uppermost branches. Ten trees of each spe-
cies were cored at 20 cm above the ground for age
determination (P. uviferum: 27–89 years, F. cupressoides:
25–180 years). Cone abundance was estimated directly
and visually by the proportion of the crown bearing cones.
Three classes were recorded with cone abundance being
considered low, medium or high when the proportion of
the crown bearing cones was 0–20 %, 21–50 % or more
than 50 %, respectively.
This information was recorded three times a year (spring,
summer and autumn) and during three successive years
from September 1995 to May 1998. At each observation
247
 J. Grosfeld, D. Barthélémy / C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 245–250

Figure 2. Morphology of seed (a, b) and pollen-bearing (c, d) cones in F. cupressoides (left) and P. uviferum (right)
a. Seed cone before opening. b. Mature seed cone after opening. c. Pollen-bearing cone before pollination. d. Scar of fallen pollen-bearing cone.

period, branches bearing cones were collected for detailed acteristic round scar (figure 2). The identification of these
examination in order to identify scars of fallen pollen- morphological features helps to determine the expression
bearing cones or seed cones. of the sexuality in previous years.
In addition, the expression of the sexuality was observed, During this study, production abundance of seeds and
respectively, for 385 and 532 mature individuals of P. pollen-bearing cones was low for the two species and two
uviferum and F. cupressoides observed in other represen- kinds of individuals (table I). Most of the individuals pro-
tative areas from their natural distribution in Argentina duced cones in only one year while very few trees pro-
(latitude and elevations of these sites ranging between 41° duced reproductive organs every year during the observa-
46’S and 42° 36’S and between 400 and 1 100 m, respec- tion period (table II).
tively). Complementary observations were made in some
Chilean native forests.
4. Discussion and conclusion
3. Results Our data present evidence that P. uviferum and F. cupres-
soides are dioecious species. One has to discard that
For both species, all observed reproductive organs were dioecy in these species is a transitory character and that it
either pollen-bearing cones or seed cones and no bisexual changes with tree age, as the specimens studied belong to
cone was recorded. Only one specimen of F. cupressoides
developed pollen-bearing and seed cones simultaneously
each year of observation. For all other individuals of both
Table I. Cone production abundance*.
species, pollen-bearing cones and seed cones were always
borne on different individuals. For all trees that were P. uviferum F. cupressoides
followed for three successive years, no change in pollen or Abundance Male Female Male Female
seed cone production was observed. Therefore both spe- high 5.4 (3) 0.0 (0) 6.8 (3) 3.6 (2)
cies studied may be considered to be dioecious. medium 10.7 (6) 5.2 (3) 13.6 (6) 21.4 (12)
Reproductive organs are always found in a terminal low 83.9 (47) 94.8 (55) 79.5 (35) 75.0 (42)
position on the ultimate branching order.
* Percentage (and total number) of individuals per class of cone
Seed cones are woody and remain attached to the plant production abundance (low = 0–20 %, medium = 21–50 % or high >
for a long time, sometimes more than 8 years. Pollen- 50 %) and according to tree types (male or female) and species for the
bearing cones are shed after pollination and leave a char- three years of observation.

248
 J. Grosfeld, D. Barthélémy / C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 245–250

Table II. Number of years with cone production during the observa-
tion period*.
P. uviferum F. cupressoides
Years 0 1 2 3 0 1 2 3
Male 12 66 16 6 14 64 18
Female 18 56 22 4 22 68 10
* Percentage of male or female individuals of Pilgerodendron
uviferum (left) and Fitzroya cupressoides (right) according to the
number of years they produced cones during the three years of
observation.
different age groups. Even though one specimen of F.
cupressoides developed pollen-bearing and seed cones
simultaneously each year of observation, it seems to rep-
resent an exceptional case, as this can also occur in the
dioecious species Araucaria araucana, another conifer
from Patagonia [32].
Except for most species of Juniperus L., Diselma archeri
Hook. f. and Microbiota decussata Kom. [13, 14, 19, 24,
25, 27, 29, 31, 33], Cupressaceae species are normally
considered to be monoecious. Our present work and data
concerning Austrocedrus chilensis [11] show that all
Cupressaceae species of South America are dioecious.
The discrepancies found in the literature, identifying
both the species studied here as dioecious or monoecious
might be due to the following reasons.
1) In most works cited, a great confusion arises from a
misuse of the botanical terminology for describing the
reproductive organs themselves (i.e. the use of the term
‘flower’ for the reproductive organ of Gymnosperms) or
the distribution of reproductive structures among the indi-
viduals of a species. Thus some authors [13–15, 19–24]
refer to ‘monoecious or dioecious flowers’. However,
these terms should not be applied to the ‘flower’ [34], but
to the distribution of unisexual ‘flowers’ (strobili or cones
in Coniferales) among the individuals of the same species
[35, 36]. The same confusion in terminology is found for
description at the higher taxa level, such as the family
Cupressaceae and the order Coniferales, as was indicated
by Brion et al. [11].
2) The determination of the monoecious or dioecious state
from only a few specimens cultivated in Europe out of their
4 native area ([22] as suggested in [23]), from material the
0 origin of which is not clarified [23] or from perhaps
exceptional or teratological material such as specimens
presenting ‘hermaphrodite flowers’ [22] which, generally,
is not the normal condition for the reproductive organs of
Gymnosperm species [10].
3) The successive citation of bibliographical data without
confirmation by direct observations from living or newly
collected material (i.e. the description of ‘hermaphrodite
flowers’ in Fitzroya cupressoides cited by Elwes and Henry
in 1912 [22] and then re-cited by many later authors with
[23] or without [13] reference to the original work. Fur-
thermore, it is noticeable that most of the cited literature
consists of handbooks or floras which raises concerns
about the statistical value of the data as compared to
peer-reviewed articles.
As both species were observed in various growth con-
ditions and locations in their natural area, it seems likely
that dioecy in P. uviferum and F. cupressoides is not
exclusive to the specimens studied, but a characteristic of
these species. This feature is important for the manage-
ment and conservation of these threatened species, and
also for the understanding of the evolution and phylogeny
in the Cupressaceae whose relationships are still not clear,
especially for the South American species [37].
Acknowledgements. We thank D. Auclair, C. Brion,
J. Puntieri and two anonymous reviewers for useful
comments on the manuscript, Pr. A. Bell for his revision
of the English version and the Administración de
Parques Nacionales for allowing us access to the sam-
pling areas. This study was supported by the Secretaría
de Investigación, Universidad Nacional del Comahue,
Argentina (Project B-704 UNC), and CONICET of
Argentina (J. Grosfeld postgraduate fellowship).

References
[1] Veblen T.T., Delmastro R.J., Schlatter J.E., The conservation of
Fitzroya cupressoides and its environments in southern Chile, Environ.
Conserv. 3 (1976) 291–301.
[2] Veblen T.T., Ashton D.H., The regeneration status of Fitzroya cupres-
soides in the Cordillera Pelada, Chile. Biol. Conserv. 23 (1982) 141–161.
[3] Donoso C., Bosques templados de Chile y Argentina. Variación,
estructura y dinámica. Ecología Forestal, Ed. Universitaria, Conaf, San-
tiago, Chile, 1993.
[4] Lara A., Villalba R.A., 3 620-year temperature record from Fitzroya
cupressoides tree rings in southern South America, Science 260 (1993)
1104–1106.
[5] Moore D.M., Flora of Tierra del Fuego, Missouri Botanical Garden,
1983.
[6] Veblen T.T., Burns B.R., Kitzberger T., Lara A., Villalba R., The
ecology of the conifers of southern South America, in: Enright N.J.,
Hill R.S. (Eds.), Ecology of Southern Conifers, Melbourne University Press,
Melbourne, 1995, pp. 120–155.
[7] Szeicz J.M., Growth trends and climatic sensitivity of trees in the
North Patagonian rain forest of Chile, Can. J. For. Res. 27 (1997) 1003–
1014.
[8] Parker T., Donoso C., Natural regeneration of Fitzroya cupressoides
in Chile and Argentina, For. Ecol. Manage. 59 (1993) 63–85.
[9] CITES Secretariat, Checklist of CITES species: a reference to the
appendices to the Convention on International Trade in Endangered
Species of Wild Fauna and Flora, CITES Secrétariat, Genève, 1998.
[10] Gifford E.M., Foster A.S., Morphology and Evolution of Vascular
Plants, 3d ed., W.H. Freeman and Co., New York, 1988.
[11] Brion C., Grigera D., Rosso P., The reproduction of Austrocedrus
chilensis (D. Don) Florin et Boutleje, C. R. Acad. Sci. Paris Serie III 316
(1993) 721–724.
[12] Castor C., Cuevas J.G., Arroyo M.T.K., Rafii Z., Dodd R.,
Penaloza A., Austrocedrus chilensis (D. Don.) Pic-Ser. et Bizz. (Cupres-
saceae) from Chile and Argentina - monoecious or dioecious? Rev.
Chilena Hist. Nat. 69 (1996) 89–95.
[13] Dallimore W., Jackson A.B., A Handbook of Coniferae Including
Ginkgoaceae, Edward Arnold Ltd., London, 1954.
[14] Den Ouden P., Boom B.K., Manual of cultivated conifers, Marti-
nus Nishopk, The Hague, 1965.

249
 J. Grosfeld, D. Barthélémy / C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 245–250
[15] Hoffman A.J., Flora silvestre de Chile. Zona austral, Ed. Fundación
Claudio Gay, Santiago, Chile, 1982.
[16] Dimitri M.J., Leonardis J., Binoli J.S., El nuevo libro del árbol:
especies forestales de la Argentina occidental, Vol. 1, Ed. El Ateneo,
Buenos Aires, 1997.
[17] Brion C., Grigera D., Puntieri J.G., Calvello S., Flora de Puerto
Blest y sus alrededores, Ed. Educo, Neuquén, 1998.
[18] Covas G., Flora fanerogámica Argentina, fascículo 4., ProFlora,
CONICET, Buenos Aires, Argentina, 1995.
[19] Barret W., Gymnospermae. Coniferae, in: Correa M. (Ed.), Flora
Patagónica, Parte I, Col. Cient., INTA, Buenos Aires, 1998, pp. 358–372.
[20] Muñoz Schick M., Flora del Parque Nacional Puyehue, Univer-
sidad Austral de Chile, Santiago, Chile, 1980.
[21] Marticorena C., Rodríguez R., Flora de Chile. Vol. 1, Pteridophyta-
Gymnospermae, Universidad de Concepción, Concepción, 1995.
[22] Elwes H.J., Henry A., Trees of Great Britain and Ireland VI,
privately printed, Edinburg, 1912.
[23] Sahni B., Singh T.C.N., Notes on the vegetative anatomy and
female cones of Fitzroya patagonica (Hook.), J. Ind. Bot. 10 (1931) 1–20.
[24] Pardé L., Les conifères, La Maison rustique, Paris, France, 1946.
[25] Gaussen H., Les Cupressacées, Les Gymnospermes actuelles et
fossiles, tome II, Fac. des sciences, Toulouse, 1968.
[26] Tortorelli L.A., Maderas y bosques argentinos, Editorial Acme,
Buenos Aires, 1956.
[27] Callen G., Les conifères cultivés en Europe, tomes I y II, Baillière,
Paris, 1976.
250
[28] Rodríguez R., Matthei O., Quezada M., Flora arbórea de Chile,
Ed. Universidad de Concepción, Concepción, 1983.
[29] Welch H.J., The Conifer Manual, Vol. 1, Kluwer Academic Pub-
lisher, Dordrecht, Boston, 1991.
[30] Donoso C., Cortes M., Soto L., Antecedentes sobre semillas y
germinación de alerce, ciprés de las Guaytecas, ciprés de la cordillera y
tineo, Bosques 3 (1980) 96–109.
[31] Konar R.N., Investigation on the development of the male cones in
Fitzroya cupressoides (Mol.) Johnst. and Pilgerodendron uviferum (Don.)
Flor, Phytomorphology 12 (1962) 190–195.
[32] Grosfeld J.E., Barthélémy D., Brion C., Architectural variations in
Araucaria araucana (Molina) K. Koch (Araucariaceae) in its natural habi-
tat, in: Kurmann M.H., Hemsley A.R. (Eds.), The Evolution of Plant
Architecture, Royal Botanic Gardens, Kew, 1999, pp. 109–122.
[33] García Esteban L., Guindeo Casasus A., Palacios de Palacios P.,
Maderas de coníferas. Anatomía de géneros, Fundación Conde del Valle
de Salazar, Madrid, 1996.
[34] Lawrence G.H., Taxonomy of Vascular Plants, MacMillan Pub-
lisher Co., New York, 1951.
[35] Font Quer P., Diccionario de botánica, Ed. Labor, Barcelona,
Spain, 1977.
[36] Gatin C.L., Dictionaire de botanique, Lechevalier, Paris, 1975.
[37] Gadek P.A., Alpers D.L., Heslewood M.M., Quinn C.J., Relation-
ships within Cupressaceae sensu lato: a combined morphological and
molecular approach, Am. J. Bot. 97 (2000) 1044–1057.