Forest Ecology and Management 303 (2013) 91–97

Contents lists available at SciVerse ScienceDirect

Forest Ecology and Management

journal homepage: www.elsevier .com/locate / foreco

Selecting for rust (Puccinia psidii) resistance in Eucalyptus grandis in SãoPaulo State, Brazil

0378-1127/$ - see front matter � 2013 Elsevier B.V. All rights reserved.http://dx.doi.org/10.1016/j.foreco.2013.04.002

⇑ Corresponding author at: Instituto de Pesquisas e Estudos Florestais (IPEF),Avenida Pádua Dias 11, Caixa Postal 530, CEP 13400-970, Piracicaba, SP, Brazil. Tel.:+55 19 34351681.

E-mail address: paulohenrique@ipef.br (P.H.M. Silva).

Paulo H.M. Silva a,b,⇑, Aline C. Miranda a,c, Mario L.T. Moraes c,d, Edson L. Furtado d, José Luiz Stape e,Clayton Alcarde Alvares a, Paulo Cesar Sentelhas f, Edson S. Mori d, Alexandre M. Sebbenn g

a Instituto de Pesquisas e Estudos Florestais (IPEF), Avenida Pádua Dias 11, Caixa Postal 530, CEP 13400-970, Piracicaba, SP, Brazilb Faculdade de Ciências Agrárias e Veterinárias – Campus de Jaboticabal (UNESP – FCAV), CEP 14884-900, Jaboticabal, SP, Brazilc Faculdade de Engenharia de Ilha Solteira (UNESP – FEIS), Caixa Postal 31, CEP 15385-000, Ilha Solteira, SP, Brazild Faculdade de Ciências Agronômicas de Botucatu (UNESP – FCA), Caixa Postal 237, CEP 18.603-970, Botucatu, SP, Brazile North Carolina State University, Dept. Forestry and Environmental Resources and Forest Productivity Cooperative (FPC), 3108 Jordan Hall, Raleigh, NC 27695-8008, United Statesf Escola Superior de Agricultura ‘‘Luiz de Queiroz’’ (USP – ESALQ), Av. Pádua Dias 11, Caixa Postal 9, CEP 13400-970, Piracicaba, SP, Brazilg Instituto Florestal de São Paulo, CP 1322, 01059-970 São Paulo, SP, Brazil

a r t i c l e i n f o

Article history:Received 17 January 2013Received in revised form 1 April 2013Accepted 3 April 2013Available online 10 May 2013

Keywords:Disease resistance/toleranceGenetic parametersEcological zoningAgrometeorologyTree breedingStability and adaptability analysis

a b s t r a c t

In Brazil, Eucalyptus grandis is a key species for wood production. However, some genotypes are suscep-tible to rust (Puccinia psidii), mainly in São Paulo State, where climatic conditions are favorable for itsdevelopment. Rust represents a high economic risk to forest companies because of the high potentialof damage to commercial eucalypt plantations. The aims of the present study were (i) to select progeniesof E. grandis for stability and adaptability regarding resistance to rust at different locations; (ii) comparethe selections under these different climatic conditions; and (iii) compare rust severity in the field withthe theoretical model. We observed that climatic conditions were extremely influential factors for rustdevelopment, but even under favorable conditions for disease development, we found rust-resistantprogenies. In sites unfavorable for rust development, we detected highly susceptible progenies. We foundsignificant correlation among the genetic material, environmental conditions and disease symptoms,however, we observed a simple genotype-environmental interaction and significant genetic variabilityamong the progenies. The average heritability was high among the progenies in all sites, indicatingsubstantial genetic control for rust resistance. We also observed a good relationship between rust sever-ity in the field and the theoretical model that considered annual average temperature and leaf wetness.

� 2013 Elsevier B.V. All rights reserved.

1. Introduction

Hundreds of eucalypt species are endemic to Australia andnearby islands and commercial eucalypt plantations have greatimportance around the world. However, only a few eucalypt spe-cies and their hybrids are significantly used in plantations world-wide (Harwood, 2011; Potts and Dungey, 2004). Eucalyptplantations in Brazil are some of the most productive with meanannual increments of 40 m3 ha�1 yr�1 (Gonçalves et al., 2013). Thisproductivity relates to environmental conditions (Stape et al.,2008) and reflects the physiological adaptation of the geneticmaterial to various environments. To obtain high productivity,superior genotypes have been selected over many years to adapt

to environmental conditions. In addition, the sites have also beenwell managed (soil preparation, mineral fertilization, adequatespacing and weed control). However, pests and diseases can de-stroy commercial plantations or decrease their productivity.

Eucalyptus grandis W. Hill ex Maiden is one of the world’s mostimportant species in eucalypt plantations (Harwood, 2011), withexcellent genetic base available. This species was introduced inBrazil over a hundred years from different regions of Australia. E.grandis shows favorable growth and stem shape, but many of itsgenotypes are susceptible to Puccinia psidii (guava or eucalyptrust), mainly in the state of São Paulo, southeastern Brazil, wherethe eucalypt plantations plays a very important role, and where cli-matic conditions are favorable for rust development (Furtado et al.,2008).

P. psidii is native to South America (Argentina, Brazil, Colombia,Ecuador, Paraguay, Uruguay and Venezuela) and Central America(Alfenas et al., 2005) and has a wide distribution. This fungus hasbeen reported in Mexico, Cuba, the Dominican Republic, Jamaica,

92 P.H.M. Silva et al. / Forest Ecology and Management 303 (2013) 91–97

Puerto Rico, Trinidad, Florida (Coutinho et al., 1998; Booth et al.,2000) and Hawaii (Killgore and Heu, 2005), from where it wasspread throughout the Hawaiian archipelago and Japan, infectingMetrosideros polymorpha (Uchida and Zhong, 2006; Kawanishiet al., 2009). In 2010, an exotic rust species that affects Myrtaceaewas detected in Australia (Carnegie et al., 2010). This fungus wasrecognized as a taxon within the P. psidii complex, which is a threatto biosecurity in Australia (Carnegie and Cooper, 2011).

This fungus represents a high economic risk to forest companiesand threatens the biodiversity since it has a high potential to dam-age Myrtaceae family plants (Tommerup et al., 2003; Grgurinovicet al., 2006; Glen et al., 2007; Booth and Jovanovic, 2012; Mirandaet al., 2012).

In native areas of Myrtaceae species where the climatic condi-tions are favorable for rust development, the disease could be asource of pressure during the regeneration process. In the caseof eucalypts, natural regeneration is not as strong as in othergenera, such as Acacia, and specific conditions are necessary forsuccessful regeneration (Ashton, 2000; Silva et al., 2011). Thisnew pressure for eucalypts could be a cause of reduction in thegenetic base.

Rust occurs mainly in seedlings, nurseries and young trees inthe field. The fungus can be easily identified based on the intense,powdery, yellow urediniospore sporulation observed in youngplant organs, such as leaves, petioles, stems and branches. Rustattack can delay plant development, kill the shoot and cause lossof apical dominance (Ferreira, 1983). Rust rarely kills eucalypttrees, except when new shoots in a coppice or young seedlingsare severely attacked. Most commonly, plants that are attackedrecover after pustules dry, which decreases forest productivityin commercial plantations (Furtado et al., 2009) and increasesproduction costs, when a control management is required. How-ever, in native areas with Myrtaceae species, P. psidii is a quaran-tine concern, as it could damage native eucalypt communities(Park et al., 2000).

Some authors have reported genetic parameters for diseaseresistance (Mori et al., 2004; Rosado et al., 2010). The selectionfor genotypes resistant to P. psidii, requires conduction of experi-ments in multiple sites to enable better quantification of geno-type � environment effects and their possible impact on theselection and range of genotypes at different areas. The identifica-tion and selection of resistant genotypes that show stability andadaptability to respond to different environmental conditions areimportant procedures in breeding programs, given that studiesshow variation in susceptibility to rust both inter and intra treespecies (Tommerup et al., 2003; Morin et al., 2012).

The objectives of our study are: (i) to select progenies of E. gran-dis in terms of stability and adaptability regarding resistance torust in nine locations in the state of São Paulo, Brazil; (ii) to com-pare the progenies selection ranking under these different climatic

Table 1Location of the experimental sites and their climate characteristics.

Site Location (cities) Planting date Latitude (S) Longitude (W) Altitude

1 Anhembi Jun/2009 22�470 48�070 4722 Avaré Jun/2009 23�050 48�550 7663 Boa Esperançado Sul Aug/2009 21�570 48�310 4904 Cabrália Paulista Feb/2009 22�270 49�200 5395 Capão Bonito Mar/2009 24�000 48�200 7056 Itapetininga Mar/2009 23�350 48�030 6567 Itararé May/2009 24�060 49�190 7408 Lençóis Paulista Mar/2009 22�350 48�480 5509 Pratânia May/2009 22�500 48�490 685

AAT – annual average temperature; AmT – average minimum temperature; AMT – aversubtropical climates (Cwa – dry winter and Cfa – no distinguished dry season) – Cwa/A

conditions; and (iii) to compare the rust severity in the field withan theoretical model that considers annual average temperatureand leaf wetness, and to zone rust severity for the state of São Pau-lo based on the proposed model.

2. Materials and methods

2.1. Genetic material, location and characterization of experimentalareas

Progeny tests of E. grandis were established using open-polli-nated seeds from ten provenances that belong to an experimentalnetwork of the Institute of Forestry Research and Studies (Institutode Pesquisas e Estudos Florestais – IPEF). The experimental net-work is composed of nine progeny tests established in 2009. Thetrials were set up at altitudes between 472 and 766 m and lati-tudes from 21�570S to 24�060S (Table 1). The trials were establishedin a completely randomized block design with numbers of proge-nies ranging from 134 to 160, linear plots with six trees and a min-imum of four replicates.

2.2. Field methodology for disease evaluation

We evaluated the progenies individually for rust resistance andinfection severity. The evaluations were carried out during 2009and 2010 when the stands were 6–12 months old, during the ofmaximum disease severity. We evaluated the natural rust infectionand did not perform any inoculation. A scoring scale showing thepercentage of diseased plants was used (Zamprogno et al., 2008).The scale was based on criteria for shape, distribution, frequencyand plant behavior in the field:

� 0 = disease-free plant (healthy plant);� 1 = few rust pustules on leaves;� 2 = rust pustules usually sparse or occasionally abundant on

limbs and young leaves; and� 3 = pustules abundant on limbs, petioles and leaves, at the tips

of branches and the main stem and apical necrosis.

Progenies were classified according to their average scores ineach site as follows:

� 0–1 = high resistance (HR);� 1–2 = intermediate resistance (IR); and� 2–3 = low resistance (LR).

2.3. Analysis of variance

Estimates of variance components and genetic parameters wereobtained using REML/BLUP (restricted maximum likelihood/best

(m) AAT (�C) AmT (�C) AMT (C�) Rainfall (mm) Köppen classification

21.8 18.5 25.2 1300 Cwa/Aw20.3 16.4 24.0 1274 Cwa22.7 19.0 25.3 1332 Aw22.1 18.4 24.8 1400 Aw20.1 18.0 25.0 1210 Cwa20.4 16.8 23.8 1182 Cwa19.4 15.0 23.0 1549 Cfa21.8 18.1 24.7 1350 Cwa/Aw20.8 17.1 23.7 1361 Cwa

age maximum temperature; Aw – tropical savanna climate; Cwa and Cfa – humidw – intermediary areas.

Table 2Genetic parameters for the nine Eucalyptus grandis progeny tests.

Genetic parameters Values

Narrow sense individual heritability – h2a

0.14 ± 0.005

Average heritability among progenies – h2m

0.95

Coefficient of determination for the effects of plots – C2parc

0.04

Coefficient of determination for G � E interaction – C2int

0.041

Genotypic correlation for genotype � environmentinteraction – rgloc

0.78

Coefficient of individual genotypic variation – CVgi (%) 19.4

Table 4Genetic correlation in progenies of Eucalyptus grandis regarding rust in nine sites inSão Paulo State.

Site 2 3 4 5 6 7 8 9

1 0.84** 0.55** 0.87** 0.86** 0.73** 0.82** 0.87** 0.80**

2 _ 0.37** 0.74** 0.88** 0.90** 0.94** 0.83** 0.94**

3 _ 0.63** 0.43** 0.28** 0.40** 0.47** 0.38**

4 _ 0.79** 0.61** 0.73** 0.94** 0.75**

5 _ 0.81** 0.93** 0.84** 0.87**

6 _ 0.88** 0.72** 0.92**

7 _ 0.79** 0.95**

8 _ 0.82**

Sites: 1 Anhembi; 2 Avaré; 3 Boa Esperança do Sul; 4 Cabrália Paulista; 5 CapãoBonito; 6 Itapetininga; 7 Itararé; 8 Lençóis Paulista; and 9 Pratânia.** P < 0.05.

P.H.M. Silva et al. / Forest Ecology and Management 303 (2013) 91–97 93

linear unbiased prediction) mixed linear models (Resende, 2007).To assess stability and adaptability, we used the Harmonic Meanof Relative Performance of Genetic Values (HMRPGVs) method,predicted by Best Linear Unbiased Prediction (BLUP) (Resende,2004). Stability corresponds to the Harmonic Mean of Genetic Val-ues (HMGVs) across sites, while the Relative Performance of Geno-typic Values (RPGVs) shows the adaptability in relation to theaverage of each site. The stability and adaptability correspondsimultaneously to the HMRPGV.

2.4. Agrometeorology and spatial modeling

We used the model proposed by Ruiz et al. (1989) to estimaterust severity of eucalypts to zone rust severity in São Paulo State.This model is based on the annual average temperature and leafwetness duration to estimate the degree of disease infection. Thezoning of disease severity was generated by algebra techniques(Burrough and McDonnell, 1998; Theobald, 2007), which consid-ered the ranges of annual average temperature (AAT, estimated inthe model proposed by Alvares et al. (2012)), and leaf wetness dura-tion (LWD, estimated in the model proposed by Hamada et al.,2008), which computes LWD as a function of annual relative humid-ity (ARH). We obtained the ARH map for São Paulo State by usingaverage historical data from the National Institute of Meteorology(INMET) (Brazil, 1992) and Food and Agriculture Organization fromthe United Nations (FAO/ONU) (FAO, 2001), and geostatistical pro-cedures similar to those described in Alvares et al. (2011).

Table 3Ranking of the best 20 Eucalyptus grandis progenies regarding rust resistance in each site aadaptability simultaneously (HMRPGV).

Rank Sites

1 2 3 4 5 6

1 43 30 44 41 41 432 66 29 41 43 15 663 44 43 43 106 14 144 14 114 29 44 114 445 106 106 66 66 66 306 41 44 106 14 30 297 114 41 114 114 27 158 30 66 30 111 10 1119 29 141 14 15 44 114

10 15 14 152 160 111 2211 13 152 27 50 43 4112 139 103 139 10 106 10613 50 77 111 151 151 13914 103 104 15 103 29 6415 5 27 13 29 145 7616 28 144 10 68 21 15117 68 98 160 21 152 6218 97 99 76 139 107 15219 98 139 99 28 17 6920 27 163 28 30 163 107

3. Results

The analysis of variance showed highly significant differencesfor all effects (sites, progenies and G � E). All the studied sitesshowed low individual narrow sense heritability and free interac-tions with the sites. The average heritability among the progenyin all sites was high (h2

m = 0.95), indicating a strong genetic controlof the studied trait and the possibility for genetic improvement(Table 2). The coefficient of individual genetic variation was 19.4%,indicating the presence of genetic variability among progenies.

The 20 best progenies in each site were selected and eight ofthem occurred in all studied sites, including the joint analysis ofall sites (Table 3).

In the pairwise analysis between sites, highly significant geneticcorrelations were observed for eight sites (Table 4). Only site num-ber 3 (Boa Esperança do Sul) showed low pairwise genetic correla-tion, mainly for sites with different climatic classifications.Additionally, we observed variation in the average rust scores forprogenies under different climatic conditions and provenance Fshowed more susceptibility to rust in all sites (Fig. 1). Sites withhigh temperature showed lower rust severity and lower heritabil-ity coefficient (Table 5). We detected a linear relationship betweenannual average temperature and the mean rust severity (rustscore), also between the severity and the heritability (Fig. 2).

In São Paulo State, eucalypts rust severity clearly tends to re-duce from east to west and from south to north (Fig. 3), due to

nd all sites together based on stability (HMGV), adaptability (RPGV) and stability and

Joint

7 8 9 HMGV RPGV HMRPGV

43 43 41 43 43 4344 114 43 41 41 4166 14 44 44 44 4414 41 114 114 114 11441 111 29 66 66 6629 13 151 29 29 14

111 5 106 14 14 29114 66 15 106 30 106107 106 66 30 106 30

22 28 139 111 111 1115 30 163 15 15 151

28 103 30 151 151 1555 163 22 139 139 139

106 151 13 152 152 15298 107 107 107 107 107

163 64 164 163 163 16330 140 14 27 27 16021 44 27 13 160 2715 152 5 5 13 1317 104 103 103 5 5

Fig. 1. Average rust scores of Eucalyptus grandis progenies and provenances regarding resistance in nine sites in São Paulo State (note: provenance D had poor germination).

94 P.H.M. Silva et al. / Forest Ecology and Management 303 (2013) 91–97

Table 5Low to high rust resistance scores (%) of Eucalyptus grandis progenies, average rust score, Köppen classifications and heritability for nine sites in São Paulo State.

Classification Sites LR (%) IR (%) HR (%) ARS Köppen classification h2a h2w

a h2f

a

1 Pratânia 29.2 63.0 7.8 1.69 Cwa 0.46 0.34 0.812 Itararé 18.8 55.6 25.6 1.42 Cfa 0.32 0.22 0.723 Capão Bonito 10.3 56.4 33.3 1.29 Cwa 0.35 0.26 0.754 Itapetininga 15.7 44.8 39.6 1.28 Cwa 0.39 0.29 0.865 Avaré 8.8 38.8 52.5 1.11 Cwa 0.33 0.23 0.816 Lençóis Paulista 0.7 14.6 84.7 0.51 Cwa/Aw 0.30 0.21 0.827 Anhembi 0.7 13.7 85.6 0.50 Cwa/Aw 0.22 0.15 0.608 Cabrália Paulista 0.0 8.8 91.2 0.36 Aw 0.22 0.15 0.719 Boa Esperança do Sul 0.0 0.7 99.3 0.18 Aw 0.06 0.04 0.30

LR = low resistance; IR = intermediate resistance; HR = high resistance; ARS = average rust score; AAT = annual average temperature; h2 = individual heritability; h2w = within

progeny heritability; h2f = average among progenies.

a Miranda et al. (2012).

Fig. 2. Relationships between annual average temperature and mean rust severity (rust score) and between rust severity and individual heritability.

Fig. 3. Ecological zoning for eucalypt rust severity in São Paulo State and experimental sites.

P.H.M. Silva et al. / Forest Ecology and Management 303 (2013) 91–97 95

96 P.H.M. Silva et al. / Forest Ecology and Management 303 (2013) 91–97

the combination of climatic factors, such as temperature andhumidity.

4. Discussion

Based on Köppen climatic classification, sites with an Aw classi-fication showed lower rust occurrence. Climatic conditions play animportant role in the disease development (Ruiz et al., 1989). How-ever, in favorable conditions for rust development, such as themunicipalities of Pratânia and Itararé, we found rust-tolerant prog-enies, while in sites that are unfavorable for rust development,such as Boa Esperança do Sul and Cabrália Paulista, we observedrust-susceptible progenies (Fig. 1).

We observed high heritability among the progenies, i.e., proge-nies show stable behavior regarding rust susceptibility. However,even in highly infested sites and progenies classified as rust-sus-ceptible, we found some rust-tolerant trees. Morin et al. (2012) re-ported great variation in rust susceptibility inter and intra species.Therefore, if more replicate plants per species are studied, thechances to find different behaviors inter species increase.

We observed a low G � E interaction and high genetic correla-tion between pairwise sites (0.78), revealing a simple type of inter-action (Vencovsky and Barriga, 1992). The high values of thecoefficient of genetic variation indicate the existence of genetic dif-ferences among the progenies. The high value for the average her-itability among the progeny confirms the possibility to improve thestudied population. We found heritability values among progenieshigher than those reported in the literature for rust susceptibilityin eucalypts (Mori et al., 2004; Martins et al., 2006).

We verified a slight variation in the order of the progeniesaccording to the environment, and the low variation observed indi-cates good stability in response to environmental variations. Eightof the 20 progenies showed the best rust tolerance among the ninesites (14, 30, 41, 43, 44, 66, 106 and 114). These findings indicatethe predictability of the material in different environmental condi-tions, and progenies highlighted in the HMRPGV analysis, can beselected in various environments and will show similar G � Einteraction. The small standard deviation of genotype performanceand the great HMGV observed among environments imply a simpleselection of progenies for resistance and stability should be possi-ble (Oliveira et al., 2005).

Correlations between the sites were high, except for correlationsinvolving sites with Cwa and Cfa climates and site 3 (Boa Esperançado Sul), which was the hottest site in our experimental network.This indicates that the selection for any of the sites, except for site3, may result in a good correlated response in another site, evenunder different climatic conditions. Site 3 has the highest annualaverage temperature, which is not a favorable environment for rustdevelopment (Furtado et al., 2008). Temperature is an importantfactor in the epidemiology of this disease (Ruiz et al., 1989), how-ever, leaf wetness duration and relative humidity also play animportant role. Rust can develop within a relatively wide tempera-ture range, but extreme fluctuations are unfavorable for its develop-ment (Moraes et al., 1982; Ferreira, 1983; Dianese et al., 1986).

Another factor that hampers genetic conservation is linked tothe trees’ age since rust occurrence is more common in youngeucalypts, until one and half years of age (Ferreira, 1983). There-fore, in adult trees, determining resistance is not easy. Further-more, this disease shows rapid development that can breakthrough tree resistance during years of cultivation (Samils et al.,2011). This process most likely occurs quickly where there is high-er genetic variability of the fungus, leading to a greater recombina-tion potential among pathogen genotypes and generating newvirulent races (Graça et al., 2011). Genetic variability is commonlylow in sites where P. psidii was recently introduced (Zhong et al.,

2011). Graça et al. (2011) observed in Brazil a considerable geneticrust diversity, which is strongly related to host genotypes. There-fore, commercial eucalypt plantations with a single genotype(clone) could result in unintentional selection and reproductionof specific pathogen variability that can overcome tree resistance.

Knowing the ecological zoning of eucalypts rust is important fordetermining the most appropriate breeding strategy. This zoningcan provide useful information by indicating classes of diseaserisks and by addressing the possible effects of climatic changeson disease occurrence (Masson et al., 2007; Booth and Jovanovic,2012). Therefore, plantations should be further grouped by envi-ronment because in specific regions, rust selection is fundamental,while in other regions, genetic material associated with other eco-nomic interests may be lost, if intense selection for rust resistanceis applied.

In our study, the open pollinated progenies showed stablebehavior to rust susceptibility, simple G � E interaction, high cor-relations among sites (with same climatic classification) and highheritability. Therefore, we can maximize improvements to rust tol-erance of the population by breeding selected trees for the siteswith Cwa and Cfa climates and low annual average temperature(approximately 20 �C), which were classified in our study as regionof high rust severity.

Acknowledgements

We wish to thank Arborgen, ArcelorMittal (Aperan), Cenibra,Conpacel, Duratex, Eucatex, Fibria, Forestal Oriental, Jari, Lwarcel,Masisa, Palmasola, Stora Enso and Suzano (all companies associ-ated with the Genetic Improvement Program in IPEF), Universityof São Paulo – USP/ESALQ, São Paulo State University – UNESP, FA-PESP for their support and the reviewers and editors for all the con-tributions that improved the manuscript.

References

Alvares, C.A., Gonçalves, J.L.M., Vieira, S.R., Silva, C.R., Franciscatte, W., 2011. Spatialvariability of physical and chemical attributes of some forest soils insoutheastern of Brazil. Sci. Agric. 68, 697–705.

Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonçalves, J.L.M., Modeling monthly meanair temperature for Brazil. Theor. Appl. Climatol. 110, 1–21, <http.//dx.doi.org/10.1007/s00704-012-0796-6>.

Ashton, D.H., 2000. Ecology of eucalypt regeneration. CSIRO, In: Keane, P.J., Kile, G.A., Podger, F.D., Brown, B.N. (Eds.), Disease and Pathogens of Eucalypts,Camberra.

Alfenas, A.C., Zauza, E.A.V., Wingfield, M.J., Roux, J., Glen, M., 2005. Heteropyxisnatalensis, a new host of Puccinia psidii rust. Aust. Plant Path. 34, 285–286.

Booth, T.H., Old, K.M., Jovanovic, T., 2000. A preliminary assessment of high riskareas for Puccinia psidii Eucalyptus rust in the Neotropics and Australia. Agr. Eco.Env. 82, 295–301.

Booth, T.H., Jovanovic, T., 2012. Assessing vulnerable areas for Puccinia psidiiEucalyptus rust in Australia. Aust. Plant Path. 41, 425–429.

Brasil, 1992. Climatological Normal 1961-1990. SPI/EMBRAPA, Brasília.Burrough, P.A., McDonnell, R.A., 1998. Principles of Geographical Information

Systems. Oxford University Press, New York.Carnegie, A.J., Lidbetter, J.R., Walker, J., Horwood, M.A., Tesoriero, L., Glen, M., Priest,

M.J., 2010. Uredo rangelii, a taxon in the guava rust complex, newly recorded onMyrtaceae in Australia. Aust. Plant Path. 39, 366–463.

Carnegie, A.J., Cooper, K., 2011. Emergency response to the incursion of an exoticmyrtaceous rust in Australia. Aust. Plant Path. 40, 346–359.

Coutinho, T.A., Wingfield, M.J., Alfenas, A.C., Corus, P.W., 1998. Eucalyptus rust: adisease with the potencial for serious international implications. Plant Dis. 82,819–825.

Dianese, J.C., Haridasan, M., Moraes, T.S.A., 1986. Screening Eucalyptus species forrust resistance in Bahia. Brazil. Trop. Pest Manage. 32, 292–295.

Ferreira, F.A., 1983. Ferrugem do eucalipto. Rev. Árv. 7, 91–109.Furtado, E.L., Santos, C.A.G., Masson, M.V., 2008. Impacto potencial das mudanças

climáticas sobre a ferrugem do eucalipto no Estado de São Paulo. In: Ghini R.,Hamada E. (Eds.), Mudanças Climáticas. Impactos Sobre Doenças de Plantas noBrasil. Embrapa Informação Tecnológica, pp. 273–286.

Furtado, E.L., Dias, D.C., Ohto, C.T., Rosa, D.D., 2009. Doenças do Eucalipto no Brasil,p. 74.

Glen, M., Alfenas, A.C., Zauza, E.A.V., Wingfield, M.J., Mohammed, C., 2007. Pucciniapsidii a threat to the Australian environment and economy – a review. Aust.Plant Path. 36, 1–16.

P.H.M. Silva et al. / Forest Ecology and Management 303 (2013) 91–97 97

Gonçalves, J.L.M., Alvares, C.A., Higa, A.R., Silva, L.D., Alfenas, A.C., Stahl, J., Ferraz,S.F.B., Lima, W.P., Brancalion, P.H.S., Hubner, A., Bouillet, J.P.D., Laclau, J.P.,Nouvellon, Y., Epron, D., 2013. Integrating genetic and silvicultural strategies tominimize abiotic and biotic constraints in Brazilian eucalypt plantations. ForestEcol. Manage. 301, 6–27.

Graça, R.N., Alfenas, A., C. Ross-Davis, A.L. Klopfenstein, Ned. Kim, M.-S. Peever, T.L.,Cannon, P.G., Uchida, J.Y., Kadooka, C.Y., Hauff, R.D., 2011. Multilocus genotypesindicate differentiation among Puccinia psidii populations from South Americaand Hawaii. In: Fairweather, Lou, M., Patsy, P. (Eds.), Proceedings of the 58thAnnual Western International Forest Disease Work Conference, 2010 October4–8, Valemount, B.C. Flagstaff, A.Z. U.S. Department of Agriculture, ForestService, AZ Zone Forest, Health. pp. 131–134.

Grgurinovic, C.A., Walsh, D., Macbeth, F., 2006. Eucalyptus rust caused by Pucciniapsidii and the threat it poses to Australia. OEPP/EPPO Bull. 36, 486–489.

Hamada, E., Ghini, R., Fernandes, J.L., Pedro Júnior, M.J., Rossi, P., 2008. Spatial andtemporal variability of leaf wetness duration in the State of São Paulo. Brazil.Sci. Agric. 65, 26–31.

Harwood, C., 2011. New introductions – doing it right. In: Walker (Ed.), Developing aEucalypt Resource. Learning from Australia and elsewhere Wood TechnologyResearch Centre, University of Canterbury, Christchurch, New Zealand. pp. 125–136.

Kawanishi, T., Uematsu, S., Kakishima, M., Kagiwada, S., Hamamoto, H., Horie, H.,Namba, S., 2009. First report of rust disease on Ohia and the causal fungus,Puccinia psidii, in Japan. J. Gen. Plant Path. 75, 428–431.

Killgore, E.M., Heu, R.A., 2005. Ohia rust Puccinia psidii Winter. New Pest Advisory05–04. Hawaii Department of Agriculture.

Martins, I.S., Martins, R.C.C., Pinho, D.S., 2006. Alternativas de índices de seleção emuma população de Eucalyptus grandis Hill ex Maiden. Cerne 12, 287–291.

Masson, V.M., Ohto, C.T., Furtado, E.L., Silva, A.S., 2007. Zoneamento climático doeucalipto no estado de São Paulo visando o controle da ferrugem. Sum. Phys. 33,67.

Miranda, A.C., Moraes, M.L.T., Mori, E.S., Tambarussi, E., Furtado, E.L., Silva, P.H.M.,Sebbenn, A.M., 2012. Heritability for resistance to Puccinia psidii Winter rust inEucalyptus grandis Hill ex Maiden in Southwestern Brazil. Tree Genet. Gen.http://dx.doi.org/10.1007/s111295-012-0572-x.

Moraes, T.S.A., Gonçalves, E.L., Resende, G.C., Mendes, C.J., Suiter-Filho, W., 1982.Evolução da ferrugem causada pela Puccinia psidii WINTER em Eucalyptus spp.IPEF. Circ. Téc. 144, 1–12.

Mori, E.S., Bertoncini, G., Zimback, L., Mello, E.J., 2004. Genetic variability ofEucalyptus grandis progenies for rust resistance using quantitative trait andpopulation genetic parameters. In: International IUFRO Conference of theWP2.08.03 on Silviculture and Improvement of Eucalyptus–Eucalyptus in aChanging World, vol. 1. RAIZ Instituto de Investigação de Floresta e Papel.Aveiro – Portugal, pp. 109–115.

Morin, L., Aveyard, R., Lidbetter, J.R., Wilson, P.G., 2012. Investigating the host-rangeof the rust fungus Puccinia psidii sensulato across Tribes of the familyMyrtaceae. PLoS ONE 74, e35434. doi.10.1371/journal.pone.0035434.

Oliveira, R., Resende, M.D.V., Daros, E., Bespalhok Filho, J.C., Zambon, J.L., IDO, O.,Koehler, H., 2005. Genotypic evaluation and selection of sugarcane clones inthree environments in the state of Paraná. Crop Bree. Ap. Biot. 5, 426–434.

Park, R.F., Keane, P.J., Wingfield, M.J., Crous, P.W., 2000. Fungal Diseases of EucalyptFoliage. In: Keane, P.J.; Kile, G. A.; Podger, F./D., Brown, B.N. Dis. (Eds.), Path. ofEuc. CSIRO.

Potts, B.M., Dungey, H.S., 2004. Hybridization of Eucalyptus: Key issues for breedersand geneticists. New Forests 27, 115–138.

Resende, M.D.V., 2004. Métodos Estatísticos Ótimos na Análise de Experimentos deCampo. Embrapa Florestas, Colombo.

Resende, M.D.V., 2007. Software SELEGEN-REML/BLUP. Sistema Estatístico e SeleçãoGenética Computadorizada via Modelos Lineares Mistos. Embrapa Florestas,Colombo.

Rosado, T.B., Tomaz, R.S., Junior, M.F.R., Rosado, A.M., Guimarães, L.M.S., Araújo, E.F.,Alfenas, A.C., Cruz, C.D., 2010. Detection of QTL associated with rust resistanceusing IBD-based methodologies in exogamic Eucalyptus spp. Populations. Crop.Bree. Ap. Biot. 10, 321–328.

Ruiz, R.A.R., Alfenas, A.C., Ferreira, F.A., Vale, F.X.R., 1989. Influência da temperatura,do tempo de molhamento foliar, fotoperíodo e intensidade de luz sobre ainfecção de Puccinia psidii em eucalipto. Fitop. Bras. 14, 55–61.

Samils, B., Rönnberg-Wästljung, A.C., Stenlid, J., 2011. QTL mapping of resistance toleaf rust in Salix. Tree Genet. Gen. 7, 1219–1235.

Silva, P.H.M., Poggiani, F., Sebbenn, A.M., Mori, E.S., 2011. Can Eucalyptus invadenative forest fragments close to commercial stands? Forest Ecol. Manage. 261,2075–2080.

Stape, J.L., Binkley, D., Ryan, M.G., 2008. Production and carbon allocation in a clonalEucalyptus plantation with water and nutrient manipulations. Forest Ecol.Manage. 255, 920–930.

Theobald, D.M., 2007. GIS Concepts and ArcGIS Methods, third ed. ConservationPlanning Technologies, Fort Collins.

Tommerup, I.C., Alfenas, A.C., Old, K.M., 2003. Guava rust in Brazil – a threat toEucalyptus and other Myrtaceae. J. Forest. Sci. 33, 420–428.

Uchida, J., Zhong, S., 2006. First report of rust disease on Ohia caused by Pucciniapsidii in Hawaii. Plant Dis. 90, 524.

Vencovsky, R., Barriga, P., 1992. Genética Biométrica no Fitomelhoramento.Sociedade Brasileira de Genética, Ribeirão Preto.

Zamprogno, K.C., Furtado, E.L., Marino, C.L., Bonine, C.A., Dias, D.C., 2008. Utilizaçãode análise de segregantes agrupados na identificação de marcadores ligados agene que controlam a resistência à ferrugem Puccinia psidii Winter emEucalyptus sp. Sum. Phyt. 34, 253–255.

Zhong, S., Yang, B., Puri, K.D., 2011. Characterization of Puccinia psidii isolates inHawaii using microsatellite DNA markers. J. Gen. Plant Path. 77, 178–181.http://dx.doi.org/10.1007/s10327-011-0303-4.