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Dioecy in Fitzroya cupressoides (Molina) I.M. Johnst. and Pilgerodendron uviferum (D. Don.) Florin (Cupressaceae)
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 Pilgerodendron 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: [email protected] (D. Barthélémy).
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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 informations 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 naturelles. 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 différents et les deux espèces sont donc dioïques. On peut écarter l’hypothèse que les deux espèces sont dioïques
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 individus 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 exceptionnel 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 compréhension des relations phylogénétiques chez les Cupressaceae d’Amérique du Sud et plus généralement entre les espèces de l’hémisphère Sud.
1. Introduction
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 strobili, i.e. microsporangiate or pollen-bearing cones and megasporangiate or seed cones [10]. However for these Patagonian Cupressaceae contradictory reports exist concerning their monoecious or dioecious condition. Brion et al. [11] and Castor et al. [12] recently demonstrated that Austrocedrus chilensis is a dioecious species. Nevertheless, despite its importance for the management and conservation of these protected species, monoecious or dioecious 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 monoecious tree, but Covas [18] affirms that it is dioecious. However, Barret [19] describes it as a tree with ‘monoecious 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-
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 populations 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 centuries [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].
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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 Rodriguez [21] speak of ‘dioecious flowers’. For both species, observations on their reproductive phenology in Chilean forests revealed that seed production 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 systematically 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 northern 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 species 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
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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 examination in order to identify scars of fallen pollenbearing cones or seed cones. In addition, the expression of the sexuality was observed, respectively, for 385 and 532 mature individuals of P. uviferum and F. cupressoides observed in other representative areas from their natural distribution in Argentina (latitude and elevations of these sites ranging between 41° 46’S and 42° 36’S and between 400 and 1 100 m, respectively). Complementary observations were made in some Chilean native forests.
3. Results For both species, all observed reproductive organs were either pollen-bearing cones or seed cones and no bisexual 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 species, pollen-bearing cones and seed cones were always borne on different individuals. For all trees that were followed for three successive years, no change in pollen or seed cone production was observed. Therefore both species studied may be considered to be dioecious. Reproductive organs are always found in a terminal position on the ultimate branching order. Seed cones are woody and remain attached to the plant for a long time, sometimes more than 8 years. Pollenbearing cones are shed after pollination and leave a char-
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acteristic round scar (figure 2). The identification of these morphological features helps to determine the expression of the sexuality in previous years. During this study, production abundance of seeds and pollen-bearing cones was low for the two species and two kinds of individuals (table I). Most of the individuals produced cones in only one year while very few trees produced reproductive organs every year during the observation period (table II).
4. Discussion and conclusion Our data present evidence that P. uviferum and F. cupressoides are dioecious species. One has to discard that dioecy in these species is a transitory character and that it changes with tree age, as the specimens studied belong to
Table I. Cone production abundance*.
P. uviferum Abundance high medium low
Male 5.4 (3) 10.7 (6) 83.9 (47)
Female 0.0 (0) 5.2 (3) 94.8 (55)
F. cupressoides Male 6.8 (3) 13.6 (6) 79.5 (35)
Female 3.6 (2) 21.4 (12) 75.0 (42)
* Percentage (and total number) of individuals per class of cone production abundance (low = 0–20 %, medium = 21–50 % or high > 50 %) and according to tree types (male or female) and species for the three years of observation.
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 observation period*.
P. uviferum Years Male Female
0 12 18
1 66 56
2 16 22
F. cupressoides 3 6 4
0 14 22
1 64 68
2 18 10
3 4 0
* 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 represent 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 individuals 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
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 cupressoides 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, Santiago, 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.
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 native area ([22] as suggested in [23]), from material the 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. Furthermore, 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 conditions 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 management 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 sampling 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).
[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. (Cupressaceae) 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, Martinus Nishopk, The Hague, 1965.
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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, Universidad Austral de Chile, Santiago, Chile, 1980. [21] Marticorena C., Rodríguez R., Flora de Chile. Vol. 1, PteridophytaGymnospermae, 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.
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[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 Publisher, 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 habitat, 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 Publisher 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., Relationships within Cupressaceae sensu lato: a combined morphological and molecular approach, Am. J. Bot. 97 (2000) 1044–1057.
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 Pilgerodendron 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: [email protected] (D. Barthélémy).
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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 informations 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 naturelles. 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 différents et les deux espèces sont donc dioïques. On peut écarter l’hypothèse que les deux espèces sont dioïques
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 individus 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 exceptionnel 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 compréhension des relations phylogénétiques chez les Cupressaceae d’Amérique du Sud et plus généralement entre les espèces de l’hémisphère Sud.
1. Introduction
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 strobili, i.e. microsporangiate or pollen-bearing cones and megasporangiate or seed cones [10]. However for these Patagonian Cupressaceae contradictory reports exist concerning their monoecious or dioecious condition. Brion et al. [11] and Castor et al. [12] recently demonstrated that Austrocedrus chilensis is a dioecious species. Nevertheless, despite its importance for the management and conservation of these protected species, monoecious or dioecious 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 monoecious tree, but Covas [18] affirms that it is dioecious. However, Barret [19] describes it as a tree with ‘monoecious 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-
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 populations 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 centuries [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].
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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 Rodriguez [21] speak of ‘dioecious flowers’. For both species, observations on their reproductive phenology in Chilean forests revealed that seed production 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 systematically 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 northern 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 species 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
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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 examination in order to identify scars of fallen pollenbearing cones or seed cones. In addition, the expression of the sexuality was observed, respectively, for 385 and 532 mature individuals of P. uviferum and F. cupressoides observed in other representative areas from their natural distribution in Argentina (latitude and elevations of these sites ranging between 41° 46’S and 42° 36’S and between 400 and 1 100 m, respectively). Complementary observations were made in some Chilean native forests.
3. Results For both species, all observed reproductive organs were either pollen-bearing cones or seed cones and no bisexual 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 species, pollen-bearing cones and seed cones were always borne on different individuals. For all trees that were followed for three successive years, no change in pollen or seed cone production was observed. Therefore both species studied may be considered to be dioecious. Reproductive organs are always found in a terminal position on the ultimate branching order. Seed cones are woody and remain attached to the plant for a long time, sometimes more than 8 years. Pollenbearing cones are shed after pollination and leave a char-
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acteristic round scar (figure 2). The identification of these morphological features helps to determine the expression of the sexuality in previous years. During this study, production abundance of seeds and pollen-bearing cones was low for the two species and two kinds of individuals (table I). Most of the individuals produced cones in only one year while very few trees produced reproductive organs every year during the observation period (table II).
4. Discussion and conclusion Our data present evidence that P. uviferum and F. cupressoides are dioecious species. One has to discard that dioecy in these species is a transitory character and that it changes with tree age, as the specimens studied belong to
Table I. Cone production abundance*.
P. uviferum Abundance high medium low
Male 5.4 (3) 10.7 (6) 83.9 (47)
Female 0.0 (0) 5.2 (3) 94.8 (55)
F. cupressoides Male 6.8 (3) 13.6 (6) 79.5 (35)
Female 3.6 (2) 21.4 (12) 75.0 (42)
* Percentage (and total number) of individuals per class of cone production abundance (low = 0–20 %, medium = 21–50 % or high > 50 %) and according to tree types (male or female) and species for the three years of observation.
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 observation period*.
P. uviferum Years Male Female
0 12 18
1 66 56
2 16 22
F. cupressoides 3 6 4
0 14 22
1 64 68
2 18 10
3 4 0
* 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 represent 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 individuals 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
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 cupressoides 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, Santiago, 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.
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 native area ([22] as suggested in [23]), from material the 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. Furthermore, 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 conditions 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 management 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 sampling 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).
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