EX SITU CONSERVATION OF ARAUCARIA ANGUSTIFOLIA (BERT.) O. KTZE. IN SÃO PAULO STATE, BRAZIL¹⁰

by
Alexandre Magno Sebbenn²; Ananias de Almeida Saraiva Pontinha¹¹;
Edgar Giannotti² ; Paulo Yoshio Kageyama ¹²

INTRODUCTION

Araucaria angustifolia (Bertoloni) Otto Kuntze (Araucariaceae) or Paraná Pine is one of the rare native South American conifers. It has great economical value through wood production and also provides human and animal food. It is distributed in Brazil between latitudes 19º15´S and 31º39´S and from latitude 41º00'W to 54º30'W, and is also found in small patches in Argentina and Paraguay. The original area occupied about 200 000 km² in Brazil, mainly in the state of Paraná (40 percent of the surface), Santa Catarina (31 percent) and Rio Grande do Sul (25 percent) and in scarce patches in the south of the state of São Paulo, Minas Gerais and Rio de Janeiro (1 percent) (Carvalho, 1994). The wide distribution probably contributes to the differentiation of this species in geographic races or ecotypes (Gurgel & Gurgel, 1965). Originally, the species dominated the landscape in South Brazil, probably from the last ice age to the end of the last century. The species grows presently exclusively in the Tropical Wet Mixed Forest (Araucaria Forest), in the Alluvial (gallery), Sub-Montane, Montane and High-Montane formations, with 5-25 individuals per hectare. It is distributed between altitudes of 500 and 2 300 m, most commonly between 500 and 1 500 m. The species is long lived, reaching a mean age of 140 to 250 years with records of individuals of up to 386 years of age. A. angustifolia is dioecious, but there are reports of monoecious individual trees. Pollination is by wind, seed production occurs after 20 years of age. The seeds are self dispersed, and dispersal is limited to the neighbourhood of the mother tree, due of the high seed weight. Birds and rodents contribute to dispersion to some degree. Trees reach 10 to 35 m height and 50 to 120 cm DBH, occasionally 50 m in height and 250 cm DBH. The trunk is straight and almost cylindrical, the main trunk is 20 m or more. Initial growth is slow, subsequently reaching 30 m³/ha/year, wood is of high quality and used for construction, plywood, furniture, boxes, pencils, chipboard, etc. It also produces long fiber cellulose and paper of exceptionally high quality. The A. angustifolia seeds are a source of protein, for human, domestic and wild animal nutrition (Carvalho, 1994). A. angustifolia is the native Brazilian species most intensively used in breeding and in genetic conservation studies (Carvalho, 1994). Genetic variation has been observed among populations, and geographically delimited races have been described (Gurgel & Gurgel, 1965; Baldanzi et al. 1973; Kageyama & Jacob, 1980; Timoni et al. 1980). However A. angustifolia is still considered a "vulnerable" species (FAO, 1996). The paper will present some ex situ conservation efforts of the species in São Paulo State, Brazil.

MATERIAL AND METHODS

The Genetic Conservation Program at the São Paulo Forest Institute (PCGIF), in partnership with EMBRAPA¹³, has developed a genetic conservation program which includes sampling of A. angustifolia populations over the area of its natural occurrence. Activities include studies on physiology and genetic structure of these populations, through progeny and population tests established at the São Paulo Forest Institute Experimental Station at Itapeva, using open-pollinated seed from 15 populations occurring in four states. A total of 123 progenies were sampled, with the number of progeny per population varying from 4 to 14 (Table 1).

Variance Component Estimates

Variance components, phenotypic variation, heritability, genetic and phenotypic correlations and expected genetic gain were estimated according to standard procedures outlined e.g. in Zheng et al. (1994), SAS (1999), Namkoong (1979), and Falconer and Mackay (1998). Effective population size and probability of not capturing rare alleles, were estimated according to Crow and Kimura (1970) and Brown and Hardner (2000).

Table 1: Details of the populations and number of progeny sampled per population.

RESULTS AND DISCUSSIONS

Significant differences by the F test of the analysis of variance were found among regions, among populations, populations/region and progeny/population for all the traits, except for the survival trait for region and progeny/population. This indicate that A. angustifolia has maintained its natural genetic variability structured at several hierarchical levels. The genetic variation among regions shows that the populations of the same region are more similar than populations from distant regions, so the genetic flow among populations within regions is greater than the genetic flow among populations of distant regions. This result is in line with the "isolation by distance" theory that assumes that distant populations will have less probability of intercrossing than close populations.

The variance component attributed to regions was null for the DBH and volume, and low for height (<1 percent). The component attributed to individuals within the progeny had a high value (minimum 92 percent) followed by that attributed to populations within regions (4.9 percent) and among progeny within populations (1.7 percent). The significant genetic variations detected among populations and populations/ region for all the traits reinforces the hypothesis of Gurgel & Gurgel Filho (1973) of the existence of ecotypes or geographical races of A. angustifolia. Races or ecotypes are populations adapted to specific environmental conditions, such as climate and soils. This is likely to be caused by directional selection for adaptation to specific environments, combined, probably, with low genetic flow acting against the homogenization of populations. Selection seems to be the strongest evolutionary force, moulding the genetic variability of the A. angustifolia populations towards an optimum of adaptation, giving rise to local races, and increasing the genetic homogeneity within the populations and consequently, also the genetic divergence among populations. The genetic variance among populations/region was generally superior to genetic variance among progeny/population, suggesting a clear structuring of the populations. Similar results were observed in progeny/provenance tests by Li et al. (1993) on Picea glauca, in Canada, Zeng et al. (1994) for Pinus caribaea var bahamensis in China and Buliuckas et al. (1999) for Acer platanoides, Alnus glutinosa, Fagus sylvatica and Fraxinus excelsios in Sweden.

The high genetic variation at different hierarchical levels detected in A. angustifolia indicates that the sampling strategy adopted was efficient in retaining part of the quantitative genetic variation of the species. The high survival observed in the experiment (> 84 percent) shows that A. angustifolia presents a high genetic plasticity and adaptation potential. Therefore, the recombination of individuals from distinct regions and populations/region could widen the genetic variability and the effective size of the original populations.

In general, populations from the Southern region of Brazil (regions E and F) showed the best growth and those from the north the poorest, except for the two populations, Barbacena-MG and Vargem Grande do Sul populations which, although originating in a northern region (A and B), were classified among the five best. The differences observed in growth were possibly associated to overall climatic characteristics, regions A and B being drier than E and F regions.

All the genetic and phenotypic correlations among the traits were high (> 0.8) and statistically significant (P < 0.01). The genetic correlations were superior to the phenotypic correlations and highest for DBH and volume. Therefore, selection on one trait may also bring gains in another. The heritabilities for the traits at individual level (h²_i) and within families (h²_w), were lower (mean 0.06) than those reported in other studies on A. angustifolia (Pires et al., 1980). The low heritability observed indicated that genetic control of the traits was weak and predicted genetic gains through selection limited. However this was likely due to the fact that heritability coefficients were estimated on the genetic variation among a maximum of 14 progenies within populations.

The mean heritability at the level of progeny was higher than the heritability at individual level or within progenies, indicating the possibility of greater gains through selection among progenies. However, in this specific case, selection will be made only among progenies to maintain also the original objective of genetic conservation. Two subplots will be kept with female trees and one with male trees for the best performing progenies, and the inverse for worst performing progenies. As there are 123 progenies, 62 will be kept with two sub-plots with three female plants and one plot with three male plants and 61 with two subplots with three male plants and one plot with three female plants. The sex ratio resulting in the test will be close to 1:1 and the effective size will be maximized with the possible limits (Crow & Kimura, 1970). This selection scheme creates low genetic gains for DBH and height (< 3 percent) but reasonable gains for volume (6.7 percent) with the advantage of keeping the wide genetic base and maximized effective population size, capitalizing gains and minimizing crossing among relatives.

The effective population size varied among populations. The Ipiúna de Caldas population had the highest effective size (54) and the Caçador population had the lowest (16). However, all the populations reached more than 90 percent of expected maximum possible effective size if an infinite number of seeds (>10.0) had been collected in each progeny (N_e). Generally, the N_e was less than the minimum usually required (50) for conservation of a population in the short term (Frankel & Soulé, 1981) except for the Ipíuna de Caldas population (54). This showed that the sample scheme adopted for intra population variability conservation was insufficient. Equally, the probability of not retaining an allele with 0.05 frequency was low. The effective size of the populations was high (433) indicating together with the significant genetic variations among region for height, among populations and among populations/region, that a large proportion of A. angustifolia genetic variability will be conserved here ex situ using this scheme.

The few remaining natural A. angustifolia populations in Brazil, approximately 2 percent of the total of existing stands are generally fragmented and degraded. The reduction in the number and size of the native populations and the intensive spread of agriculture and urbanization, prevent the species from surviving or migrating in response to possible future climatic changes. In Campos do Jordão, in the Northern part of São Paulo State, the São Paulo Forest Institute lost an important A. angustifolia progeny test to fire. In situ and ex situ conservation strategies must take into account the probability of fire in addition to the reduction in the size and number of native populations, their fragmentation, and unmanaged exploitation.

The results obtained here showed that the quantitative genetic variation within the populations is smaller among progeny in the populations than between parent populations, indicating that these populations may already be suffering the negative effects of exploitation, fragmentation and isolation. If these negative influences continue, the loss of some populations can be expected coupled with loss of genetic variation in others. There is a need to introduce alternative, sustainable management measures and measures for in situ conservation of these resources. For effective conservation of the A. angustifolia genetic resources it is fundamental to delimit additional native stands of A. angustifolia for in situ conservation and to establish "gene flow corridors" between the populations. It is also necessary to assist reproduction in native populations and to carry out enrichment planting in them to avoid that due to very few individuals there will be loss of variation through genetic drift.

The in situ conservation measures should be complemented by establishing ex situ conservation stands of local population. The sampling of approximately five populations/regions, and of at least 30 progeny/population, along with replication of each of the ex situ banks in at least two localities within each region is recommended.

ACKNOWLEDGEMENTS

The authors are grateful to the technical support team for support to research at the São Paulo Forest Institute for measuring the quantitative traits in the experiment, more specifically Carlos Bagdal, Gilson Soares de Guimarães, Valdecir Benedito Ferreira, Sivaldo Alves de Freitas e Waldinei Ferreira.

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¹⁰ Received September 2001. Original language: English.
¹¹ Instituto Florestal, São Paulo, Caixa Postal 1322, 01059-970, SP.
¹² ESALQ/USP, AV. Pádua Dias, 11, CEP 13418-900, Piracicaba, SP.
¹³ Centro da Empresa Brasileira de Pesquisa Agropecuária (Brazilian Organization for Agricultural Research)