Variation in severity of target spot, caused by ...

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Australasian Plant Pathology, 2003, 32, 393–402

Variation in severity of target spot, caused by Aulographina eucalypti, in a eucalypt species and provenance trial in Victoria Angus J. CarnegieA,B,C and Philip J. KeaneA A

B

School of Botany, La Trobe University, Bundoora, Vic. 3068, Australia. Current address: Research & Development Division, State Forests of NSW, PO Box 100, Beecroft, NSW 2119, Australia. C Corresponding author; email: [email protected]

Abstract. Target spot caused by the fungus Aulographina eucalypti was assessed from spring 1990 to summer 1991 on 44 provenances of 14 Eucalyptus species to determine the variation in susceptibility to the pathogen. A disease assessment scale for target spot was developed specifically for this study based on the development of lesions caused by A. eucalypti and the proportion of leaf area affected. Significant variation was observed among the 44 provenances in both spring and summer, with provenances from E. globulus (all provenances except Eden), E. nitens, E. cypellocarpa, E. oreades, E. sieberi and E. viminalis scoring the highest for target spot. Provenances from E. quadrangulata, E. saligna, E. botryoides and E. elata all scored low for target spot, as did E. globulus provenance Eden. Variation within species for E. botryoides, E. globulus, E. nitens, E. saligna and E. viminalis was also significant. In general, variation between provenances within species was much less than variation between species. Severity of target spot on E. globulus (also assessed in winter 1990) increased from winter to spring and again from spring to summer. The pathogen was recorded on all 14 species in the trial, including two new host records. This paper also reports new host records from field collections by the first author over the past 12 years, and from examination of herbarium specimens, adding 35 new host records for A. eucalypti and five new host records for Australia. AP03403 Ae.tauJloCg. arpenhgiea uclaypit varitioniEnucalyptusp .

Additional keywords: Eucalyptus, leaf pathogen, disease assessment scale, new host records.

Introduction One of the most common and distinctive leaf diseases in eucalypt forests and plantations in south-eastern Australia is target spot caused by Aulographina eucalypti (anamorph: Thyrinula eucalypti). The pathogen has been recorded on over 40 species of Eucalyptus in Australia (Hansford 1954; Marks et al. 1982; Wall and Keane 1984; Stone et al. 1998a; Park et al. 2000) and, in native forests, is more common on species in Eucalyptus subgenus Eucalyptus (Wall and Keane 1984). The classification of the genus Eucalyptus in this paper follows Brooker (2000) and includes subgenus Corymbia (formerly a genus, Hill and Johnson 1995), subgenus Eucalyptus (formerly subgenus Monocalyptus, Pryor and Johnson 1971) and subgenus Angophora (formerly a genus, Pryor and Johnson 1971). Additional host species have been reported overseas, mainly from plantations in South Africa (Crous et al. 1989), but also from New Zealand (Dick 1982), Brazil (Ferreira 1989, in Park et al. 2000), the United Kingdom (Spooner 1981), Vietnam (Old and Yuan © Australasian Plant Pathology Society 2003

1994), Chile (Wingfield et al. 1995) and Madagascar (Crous and Swart 1995). A. eucalypti has been described in detail previously (Wall and Keane 1984). Leaf spots are roughly circular, 2–15 mm in diameter, often raised and corky, and develop only part way through the leaf lamina whether on the upper or lower surface. Lesions develop very slowly, which allows time for the formation of a cork cambium barrier, and are most evident on older leaves. Small, black, pimple-like pycnidia develop on the surface of lesions, followed by black, elongate, often-branched pseudothecia, roughly in concentric rings. The pathogen is also able to infect petioles, small branches, fruits and smooth bark (Wall and Keane 1984), and severe infection of leaves and petioles can lead to premature defoliation (Neumann and Marks 1976; Marks et al. 1982). Most reports of severe damage by A. eucalypti have been from native forests. A. eucalypti was considered the major causal agent amongst a complex of leaf pathogens that 10.1071/AP03043

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reached epidemic levels and resulted in moderate to severe defoliation of saplings and 120- to 180-year-old E. denticulata (= E. nitens) on the Errinundra Plateau in East Gippsland, Victoria, in 1974 (Neumann and Marks 1976). Species of Alternaria, Harknesia and Mycosphaerella were also associated with the defoliation. In 1973, defoliation and death of several thousand hectares of mature E. obliqua forest in several valleys in north-west Tasmania were attributed mainly to A. eucalypti with Vermisporium (= Seimatosporium) falcatum playing a minor role (Palzer 1978; Felton 1981). Target spot reached epidemic proportions during 1993 in young E. regnans regrowth in native forest in south-central Victoria (Stefanatos 1993). Damage from target spot has generally been minor in plantations. Localised outbreaks of infection caused by A. eucalypti have been recorded from eucalypt plantations in New South Wales (Gerrettson-Cornell and Dowden 1977; Stone et al. 1998a, 1998b; Carnegie 2000; Carnegie and Johnson 2004), New Zealand (Dick 1982), Chile (Wingfield et al. 1995) and Madagascar (Crous and Swart 1995). However, this pathogen has also been associated with severe leaf spotting and defoliation on E. fastigata and E. fraxinoides in South African plantations (Crous and Wingfield 1991), and is considered of economic importance due to its potential to cause extensive defoliation (Crous et al. 1989). This paper describes a disease assessment scale developed for target spot on juvenile foliage and its use to assess variation in susceptibility to the disease between 14 Eucalyptus species and 44 provenances in a 3-year-old trial in south-eastern Australia. Methods Description of trial A trial was established in October 1988 by the Department of Sustainability and Environment, Victoria, at Tostaree (37°47'S, 148°11'E), near Nowa Nowa, in south-eastern Victoria, Australia, to test 44 provenances of 14 eucalypt species for their potential for use in commercial plantations. The experimental design was a randomised complete block with 25-tree plots and five replicates. Trees were spaced 3 m × 3 m on a square grid. Results for the incidence of Mycosphaerella leaf diseases (caused by several species of Mycosphaerella) on the juvenile foliage of 35 provenances of 13 species (Carnegie et al. 1998), and the incidence and severity of Mycosphaerella leaf disease (both M. cryptica and M. nubilosa, assessed together) on nine provenances of E. globulus (Carnegie et al. 1994) have been reported previously. Disease assessment scales To develop a disease assessment scale (DAS) for target spot on eucalypts, leaves with a range of damage caused by A. eucalypti were collected from all 14 species in the trial (Table 1). These were placed into four categories (trace, low, medium, high) based on the development of leaf spots and the proportion of leaf area affected. Representative leaves were then chosen from each category to illustrate the scale of disease severity. As E. globulus was considered the most important species in the trial (because of its potential for widespread planting in southern Australia), the DAS was developed for target spot

A. J. Carnegie et al.

on leaves of this species. Five categories of infection (severity) were assessed: 0 = no infection; 1 = specks (ca. 2 mm in diameter); 2 = specks plus spots (> 2 mm in diameter); 3 = specks plus spots, some coalescing; and 4 = specks plus spots, many coalescing (Fig. 1). Assessments of target spot Severity of target spot was assessed using the above DAS. At each assessment time, a branch at or near breast height in the juvenile crown was chosen at random and the ten leaves at the tip of the branch were assessed for severity of target spot. Where there were differences in severity on the ten leaves the average severity was recorded. For E. globulus, all 25 trees in each plot were assessed, whereas only the first five trees in each plot were assessed for the remaining 13 species and 35 provenances. The trial included provenances from the four subspecies within E. globulus: subsp. bicostata, subsp. globulus, subsp. maidenii and subsp. pseudoglobulus. E. globulus was more intensely assessed because of its importance as a forestry species in south-eastern Australia. This species was assessed in winter (August 1990), spring (November 1990) and summer (February 1990), whereas the remaining 13 species were assessed in spring (November 1990) and summer (February 1991) only. Statistical analyses All data were analysed using the GLM procedure of SAS (SAS Institute Inc. 1992). Due to severe defoliation of the juvenile foliage in summer, five of the E. nitens provenances and all but one of the E. viminalis provenances could not be assessed in February. The defoliation was attributed to Mycosphaerella leaf disease but shading of lower leaves through canopy closure was also a factor (Carnegie et al. 1994, 1998) and possibly also defoliation due to target spot. For these reasons, analyses of variance were carried out on spring scores to test for variation among all 44 provenances. Analyses of variance were also carried out on summer data for all species and provenances, except E. nitens and E. viminalis, for which data for only one provenance each was available due to severe defoliation. For those species with multiple provenances (E. botryoides, E. globulus, E. nitens, E. saligna, E. sieberi and E. viminalis), separate analyses of variance were carried out on spring data to test for variation within species, and on summer data except for E. nitens and E. viminalis. For E. globulus, analyses of variance were carried out for winter, spring and summer data to test provenance by season interaction. Transformations (arcsine and log) did not improve homogeneity, and so raw scores were used in the analyses. New host records Over the past 12 years, the first author has conducted numerous surveys of eucalypt plantations, native forests and species trials in Victoria, New South Wales, Tasmania, South Australia, Western Australia and the Australian Capital Territory. Leaves collected during these surveys were examined for leaf spot fungi. During May 2003, the first author also examined specimens of A. eucalypti from herbariums VPRI and DAR for new host records. Identification of A. eucalypti from leaves was established by examination of symptoms under a dissecting microscope, and squash mounts of mature pseudothecia examined under a light microscope. A. eucalypti is a very distinctive pathogen and is easily distinguished from other common leaf spot fungi (e.g. Mycosphaerella spp.) based on leaf spot symptoms and ascospore morphology. New host records identified from these studies are reported here.

Results A. eucalypti was recorded from all 14 Eucalyptus species and 44 provenances in the trial (Appendix I). There were

Aulographina eucalypti variation in Eucalyptus spp.


Table 1. Severity of target spot (on a scale of 0–4) on 44 provenances of 14 eucalypt species recorded at Tostaree in spring and summer, showing Least Significant Differences for all provenances and for provenances within speciesA Eucalyptus species

Provenance

Mean disease severity Spring Summer

E. botryoides E. botryoides E. botryoides E. botryoides LSD for E. botryoides E. brookeriana E. cypellocarpa E. elata E. fraxinoides E. globulus ssp. maidenii ssp. pseudoglobulus ssp. globulus ssp. globulus ssp. pseudoglobulus ssp. bicostata ssp. globulus ssp. globulus ssp. globulus LSD for E. globulus E. grandis E. grandis E. nitens E. nitens E. nitens E. nitens E. nitens E. nitens LSD for E. nitens E. oreades E. quadrangulata E. saligna E. saligna E. saligna E. saligna LSD for E. saligna E. sieberi E. sieberi E. sieberi E. sieberi E. sieberi LSD for E. sieberi E. smithii E. viminalis E. viminalis E. viminalis E. viminalis E. viminalis E. viminalis E. viminalis LSD for E. viminalis

Meroo, NSW Narooma, NSW Nowa Nowa, Victoria Orbost, Victoria

0.32 0.56 0.40 0.36 (0.36)A 0.42 0.52 0.20 0.69

0.76 1.12 0.90 0.56 (0.24) 1.56 2.50 0.20 1.52

0.38 1.52 1.52 1.32 1.34 1.48 1.42 1.86 1.33 (0.27) 0.36 0.80 1.08 1.62 1.62 2.06 1.56 0.96 (0.68) 0.68 0.59 0.38 0.64 0.20 0.18 (0.93) 1.58 0.86 0.76 1.14 1.20 (1.07) 0.44 0.36 1.06 0.98 1.35 0.94 0.60 0.78 (0.61)

1.10 1.94 2.60 2.33 2.32 2.44 2.48 3.10 2.78 (0.48) 1.54 1.60 — 2.61 — — — — — 2.28 1.28 1.00 0.86 1.03 1.27 (0.29) 1.62 2.16 1.66 1.66 1.80 (0.95) 1.58 2.01 — — — — — — —

0.71

0 .65

LSD between provenance means for all provenances analysed together (P < 0.05)

Benwerrin, Victoria Mt Erica, Victoria Narooma, NSW Eden, NSW Eden, New South Wales Jeeralang, Victoria Judbury, Tasmania King Is., Tasmania Kuark, Victoria Mansfield, Victoria Otway National Park, Victoria St. Helens, Tasmania Wye River, Victoria Bulahdelah, NSW Coffs Harbour, NSW Mt Erica, Victoria Mt Kaye, Victoria Powelltown, Victoria Snobs Creek, Victoria Tallaganda, NSW Tooronga Plateau, Victoria Lithgow, NSW Albion Park, NSW Batemans Bay, NSW Beaumont, NSW Coffs Harbour, NSW Glen Innes, NSW Erica, Victoria Nowa Nowa, Victoria Nullica State Forest, NSW Scamander, Tasmania Yarram, Victoria Mt Buck, Victoria Big Badga, NSW Bruthen, Victoria Fingal, Tasmania Nowa Nowa, Victoria Silver Creek, Victoria Templestowe, Victoria Wye River, Victoria

A Figures in parentheses are Least Significant Difference (P < 0.05) between provenance means for provenances within species, analysed separately for each species. Where no LSD is shown, there were no significant differences between provenances.

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Fig. 1. Disease assessment scale developed for severity of target spot caused by Aulographina eucalypti on eucalypt leaves.

significant differences (P < 0.05) in severity of target spot in spring among the 44 provenances (Table 1). Provenances within E. globulus (all but Eden, subsp. maidenii), E. nitens (Mt Kaye, Powelltown, Snobs Creek and Tallaganda), E. sieberi (Erica) and E. viminalis (Nowa Nowa) were amongst the most severely affected by the disease. Provenances within E. botryoides (Meroo, Nowa Nowa and Orbost), E. brookeriana, E. elata, E. grandis (Bulahdelah) and E. saligna (Coffs Harbour and Glen Innes) had the lowest severities. One provenance from both E. globulus (Eden) and E. viminalis (Big Badga) were also amongst the least severely diseased.


For the majority of provenances, the severity of target spot increased from spring to summer and there were also significant differences (P < 0.05) among provenances in summer (Table 1). Provenances within E. globulus (all but Eden), E. nitens, E. sieberi (all provenances) and E. viminalis were again amongst the most severely affected. Also, provenances of E. cypellocarpa and E. oreades were amongst the most severely affected in summer. The same provenances within E. botryoides and E. elata scored the lowest for disease in summer as in spring. Significant changes in severity of target spot from spring to summer were observed in E. viminalis, Big Badga (0.36 to 2.01), E. saligna, Glen Innes (0.18 to 1.27), E. saligna, Coffs Harbour (0.2 to 1.03), E. cypellocarpa (0.52 to 2.50), E. grandis, Bulahdelah (0.36 to 1.54) and E. oreades (0.68 to 2.28). Disease severity in many provenances doubled from spring to summer, with only E. elata staying constant over both seasons. On E. globulus, disease severity increased from winter to spring, and again from spring to summer, with the highest severities on all provenances being recorded in summer (Fig. 2). Only E. globulus, E. nitens and E. viminalis showed significant (P < 0.05) variation in disease among provenances in spring, whereas in summer, E. botryoides, E. globulus and E. saligna showed significant (P < 0.05) variation in disease among provenances (Table 1). Within E. globulus, which also showed provenance variation in winter, Eden (subsp. maidenii) had significantly less disease than all other provenances, with St Helens, Wye River, Otway National Park and Judbury (all subsp. globulus) having the most severe target spot (pooling means across seasons). For E. globulus, provenances from Mansfield (subsp. bicostata) had significantly lower disease than those from St Helens. For E. nitens, Tooronga Plateau and Mt Erica had significantly less disease in spring than Snobs Creek. For E. viminalis, Big Badga and Templestowe provenances had less disease in spring than Nowa Nowa. In summer, E. botryoides provenance Orbost had significantly less disease than Narooma and Nowa Nowa, and Meroo was significantly lower than Narooma. Within E. saligna, Beaumont had significantly less disease in summer than the provenance from Glen Innes. In the assessment of target spot in the present study, A. eucalypti was isolated from two previously unrecorded hosts (E. brookeriana and E. smithii), and from four hosts on which the pathogen had not previously been reported in Australia (E. elata, E. oreades, E. quadrangulata and E. saligna). During a survey of a species and provenance trial in Victoria in December 1993, A. eucalypti was isolated from six hosts not previously recorded (E. badjensis, E. bosistoana, E. cameronii, E. dendromorpha, E. dunnii and E. melliodora), and a new host record for Australia (E. muelleriana) (Appendix I). Surveys in commercial plantations in NSW from 1996 to 2003 recorded A. eucalypti



397

3.5 Eden, NSW Severity of target spot

3 Jeeralang, Victoria 2.5

Judbury, Tasmania

2

King Is., Tasmania Kuark, Victoria

1.5

Mansfield, Victoria

1

Otway National Park, Victoria St Helens, Tasmania

0.5 0 Winter

Spring

Summer

Wye River, Victoria

Fig. 2. Severity of target spot on provenances of Eucalyptus globulus across three seasons at Tostaree. See Table 1 for E. globulus subspecies.

on E. cloeziana (Carnegie 2000), E. haemastoma, E. punctata, E. citriodora spp. variegata, and E. henryi, all new host records (Appendix I). Examination of specimens in herbariums DAR and VPRI revealed 22 hosts for A. eucalypti not previously reported (E. transcontinentalis, E. cyanophylla, E. leucoxylon, E. phaeotricha, E. polyanthemos, E. pyrocarpa, E. triflora, E. urnigera, E. tetraptera, E. grossa, E. stricklandii, E. kitsoniana, E. gunnii, E. platypus, E. citriodora, E. ficifolia, E. cordifolia, E. eremophila, E. lansdowneana, E. stricta, E. robusta and E. torquata) (Appendix I). An updated host list for A. eucalypti is provided in Appendix II. Discussion Target spot increased from winter to spring and again from spring to summer in the trial at Tostaree, which is consistent with other findings. Wall and Keane (1984) followed the development of lesions of A. eucalypti on tagged leaves of E. obliqua in Narbethong over 2 years. Lesions on the majority of leaves increased in size from June and August of one year to January and March the following year. Stone et al. (1998a) reported that fungal damage associated with A. eucalypti and other fungi increased from February of one year to July the following year. Lesions caused by A. eucalypti develop very slowly (Wall and Keane 1984) and so they are more evident on older leaves. Epidemic development of A. eucalypti is limited in winter by the availability of inoculum, which decreases at temperatures below 15°C, and the lack of young, susceptible leaves (Wall and Keane 1984) which start developing in spring. A. eucalypti is also hindered by the lack of free moisture for spore release and infection on hot, dry days in summer (Wall and Keane 1984). Therefore, epidemic development of A. eucalypti would be greatest in spring with the new leaf

flush of the host and spring rains, and would then decline as the days become hot and dry during late summer and too cold during winter. This pattern of disease development was observed in the trial at Tostaree. Wide variation in susceptibility to target spot was observed both within, and between, species at Tostaree. In general, variation between provenances within species was much less than variation between species. As disease was greatest in summer, ranking of provenances is best done with summer scores. Due to wide variation within species, it was not feasible to calculate species means for comparison of target spot amongst the 14 species. However, in general, six species had a high or relatively high ‘mean’ score for target spot in summer. These were, in decreasing order of severity, E. globulus (all provenances except Eden), E. nitens, E. cypellocarpa, E. oreades, E. sieberi and E. viminalis, all with ‘mean’ scores above 1.75 (species means of summer scores). In contrast, E. quadrangulata, E. saligna, E. botryoides and E. elata all had ‘mean’ scores below 1.30. E. brookeriana, E. fraxinoides, E. grandis and E. smithii were in the middle range with average scores in summer of 1.52 to 1.58. Crous and Wingfield (1991) reported that A. eucalypti can cause extensive defoliation to E. fraxinoides and E. fastigata in South Africa, but made no mention of damage to E. nitens, which is widely planted there, suggesting it is less susceptible to A. eucalypti. This contrasts with our findings in which E. nitens was one of the most susceptible species. Intra-species variation for severity of target spot on eucalypts has been reported previously. Significant variation in severity of A. eucalypti was reported amongst provenances of E. obliqua in a trial in Victoria (Parkin 1976). Variation amongst provenances of E. regnans and E. laevopinea was observed during assessments of fungal damage in trials in

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NSW where A. eucalypti was the main pathogen on these species (Stone et al. 1998a). Variation in severity of Mycosphaerella leaf disease and target spot was observed in a E. pilularis family trial in NSW (Carnegie and Johnson 2004). Significant variation was observed among provenances within E. botryoides, E. globulus, E. nitens, E. saligna and E. viminalis in the present study. Variation in susceptibility of provenances to leaf spot fungi has been attributed to the adaptation of the provenance to the disease in their particular environment (Carnegie et al. 1994). Those provenances originating from areas where disease is prevalent (such as in areas with a high summer rainfall) may have undergone more intense selection for resistance than those originating from areas with typically dry summers, where disease may not be important and, therefore, selection not as intense. When these latter provenances are planted in areas where the disease is common, they are likely to be severely damaged by the disease. Although the results are variable, there is some evidence for this phenomenon in the present study. For E. globulus, St Helens and Judbury in Tasmania and Mansfield in Victoria are areas that are typically too cold or too dry for significant disease development. When planted at Tostaree (an area with typically moist summers), provenances from St Helens, Judbury and Mansfield sustained high levels of target spot in the current study, and also sustained severe Mycosphaerella leaf disease (Carnegie et al. 1994). In contrast, provenances from Eden, NSW, which is in an area in the same climatic region as Tostaree and experiences typically moist summers, had low levels of both target spot and Mycosphaerella leaf disease (Carnegie et al. 1994) when planted at Tostaree. Selective breeding of resistant or tolerant genotypes is an important strategy for disease management in forestry. The use of resistant genotypes in reducing the impact of foliar pathogens has been widely discussed for eucalypts (Wilcox 1982a, 1982b; Purnell and Lundquist 1987; Carnegie et al. 1994, 1998; Dungey et al. 1997; Stone et al. 1998a; Carnegie and Ades 2002; Carnegie and Johnson 2004). E. globulus and E. nitens are the most important eucalypt species used in short rotation plantations in southern Australia and in other temperate regions of the world. Both target spot and Mycosphaerella leaf disease are considered the most important foliar diseases of these hosts in southern Australia. Studies of Mycosphaerella leaf disease on E. globulus and E. nitens have reported significant provenance and family variation within these species (Purnell and Lundquist 1987; Carnegie et al. 1994, 1998; Dungey et al. 1997). The present study showed that there was also wide variation in severity of target spot within E. globulus and E. nitens. Phenotypic correlations between severity of target spot and Mycosphaerella leaf disease on E. globulus in the trial at Tostaree were significant, more so for scores in summer (r = 0.52, P < 0.01) than in winter (r = 0.34, P < 0.05) (Carnegie


1991). Target spot was correlated only slightly with Mycosphaerella leaf disease for E. pilularis in a trial in New South Wales (Carnegie and Johnson 2004). In both these trials (Carnegie 1991; Carnegie and Johnson 2004) trees sustained more damage from Mycosphaerella leaf disease than from target spot. Susceptibility to both Mycosphaerella leaf disease and target spot has been shown to be low to moderately heritable (Dungey et al. 1997; Carnegie and Johnson 2004). Therefore, it could be feasible to select provenances within E. globulus or E. nitens that have a low susceptibility to both diseases. The present work on target spot and that by others with Mycosphaerella leaf disease indicate that breeding for resistance could be an effective tool to reduce the impact of Mycosphaerella leaf disease and target spot in Australian eucalypt plantations. The current paper reports 35 new hosts for A. eucalypti, and five host records not previously reported from Australia, from field collections and herbarium specimens. Sankaran et al. (1995) published a host list for A. eucalypti, derived solely from published records, with 49 species of Eucalyptus. The current work and other recent studies (Stone et al. 1998a; Barber et al. 2003; M. Dick, personal communication) bring the reported host range for A. eucalypti to 90 species of Eucalyptus, in E. subg. Eucalyptus, E. subg. Symphyomyrtus, E. subg. Corymbia, E. subg. Eudesmia E. subg. Alveolata, E. subg. Idiogenes and E. subg. Angophora (see Appendix II). Heather (1971) and Burdon and Chilvers (1974) reported that A. eucalypti is more common on species in E. subg. Eucalyptus in native forests. However, the current study and numerous others (e.g. Marks et al. 1982; Dick 1982; Wall and Keane 1984; Crous et al. 1989; Stone et al. 1998a) have revealed a much wider host range for the pathogen, especially from plantations. These reveal that A. eucalypti has many hosts in both E. subg. Eucalyptus and E. subg. Symphyomyrtus. Few eucalypt leaf spot pathogens have such a wide host range. M. cryptica, considered one of the most important leaf spot fungi in Australia, has a reported host range of over 50 eucalypt species in both E. subg. Symphyomyrtus and E. subg. Eucalyptus, but not in E. subg. Corymbia. Other leaf fungi with wide host ranges include Phaeophleospora epicoccoides (Park et al. 2000) and several species of Cylindrocladium (Brown and Ferreira 2000). Of these, A. eucalypti and M. cryptica are considered the most damaging in eucalypt plantations in Australia. Acknowledgments Peter Ades assisted with statistical analyses; Ian Smith and Paul Clements helped with data collection; the Department of Sustainability and Environment gave permission to assess their field trials; La Trobe University provided support during this research; and herbariums VPRI and DAR provided loans of specimens and received our collections for accession. For this we are most grateful.


References Barber PA, Smith IW, Keane PJ (2003) Foliar diseases of Eucalyptus spp. grown for ornamental cut foliage. Australasian Plant Pathology 32, 109–111. Brooker MIH (2000) A new classification of the genus Eucalyptus L’Her. (Myrtaceae). Australian Systematic Botany 13, 79–148. Brown BN, Ferreira FA (2000) Diseases during propagation of eucalypts. In ‘Diseases and pathogens of eucalypts’. (Eds PJ Keane, GA Kile, FD Podger, BN Brown) pp. 119–151. (CSIRO Publishing: Melbourne) Burdon JJ, Chilvers GA (1974) Fungal and insect parasites contributing to niche differentiation in mixed stands of eucalypt saplings. Australian Journal of Botany 22, 103–114. Carnegie AJ (1991) ‘The susceptibility of certain Eucalyptus species and provenances to infection by Mycosphaerella spp. and other leaf parasites.’ Honours Thesis, School of Botany, La Trobe University, Australia. Carnegie AJ (2000) State and company overviews of eucalypt plantation estates and pest problems — New South Wales. In ‘Proceedings of a workshop on managing pests of eucalypt plantations’. 10–11 February 2000, Department of Forestry, ANU, Canberra. (Eds H Elliot, C McArthur, R Floyd, D de Little) pp. 15–25. (CRC for Sustainable Production Forestry) Carnegie AJ, Ades PK (2003) Mycosphaerella leaf disease reduces growth of plantation-grown Eucalyptus globulus. Australian Forestry 66, 113–119. Carnegie AJ, Ades PK, Keane PJ, Smith IW (1998) Mycosphaerella diseases of juvenile foliage in a eucalypt species and provenance trial in Victoria, Australia. Australian Forestry 61, 190–194. Carnegie AJ, Johnson IA (2004) Variation among families of blackbutt (Eucalyptus pilularis) in early growth and susceptibility to damage from leaf spot fungi. Canadian Journal of Forest Research (in press). Carnegie AJ, Keane PJ (1994) Further Mycosphaerella species associated with leaf diseases of Eucalyptus. Mycological Research 98, 413–418. Carnegie AJ, Keane PJ, Ades PK, Smith IW (1994) Provenance variation in Eucalyptus globulus in susceptibility to Mycosphaerella leaf disease. Canadian Journal of Forest Research 24, 1751–1757. Crous PW, Knox-Davies PS, Wingfield MJ (1989) A summary of fungal leaf pathogens of Eucalyptus and the diseases they cause in South Africa. South African Forestry Journal 149, 9–16. Crous PW, Swart WJ (1995) Folicolous fungi of Eucalyptus spp. from eastern Madagascar: implications for South Africa. South African Forestry 172, 1–5. Crous PW, Wingfield MJ (1991) Eucalyptus leaf pathogens in South Africa: a national perspective. In ‘Proceedings of the IUFRO symposium for intensive forestry. The role of eucalypts’. Durban, South Africa. (Ed APG Schonau) pp. 749–759. Dick M (1982) Leaf-inhabiting fungi of eucalypts in New Zealand. New Zealand Journal of Forestry Science 12, 525–537. Dungey HS, Potts BM, Carnegie AJ, Ades PK (1997) Mycosphaerella leaf diseases: genetic variation in damage to Eucalyptus nitens, E. globulus and their F1 hybrid. Canadian Journal of Forest Research 27, 750–759. Felton K (1981) Eucalyptus diebacks in Tasmania. In ‘Eucalyptus dieback in forests and woodlands’. (Eds KM Old, GA Kile, CP Ohmart) pp. 51–54. (CSIRO Publishing: Melbourne) Gerrettson-Cornell L, Dowden HGM (1977) Soil and leaf fungi in a eucalypt plantation at Olney State Forest, New South Wales. Australasian Plant Pathology Society Newsletter 6, 24–25. Hansford GC (1954) Australian fungi. II. New species and revisions. Proceedings of the Linnean Society of New South Wales 79, 97–141.


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Heather WA (1971) Diseases in native forests. The Forestry Log 4, 25–27. Hill KD, Johnson LAS (1995) Systematic studies in the eucalypts. 7. A revision of the bloodwoods, genus Corymbia (Myrtaceae). Telopea 6, 173–505. Marks GC, Fuhrer BA, Walters NEM (1982) ‘Tree diseases in Victoria.’ Forests Commission Victoria Handbook No. 1, Forests Commission, Victoria Neumann FG, Marks GC (1976) A synopsis of important pests and diseases in Australian forests and forest nurseries. Australian Forestry 39, 83–102. Old KM, Yuan ZQ (1994) ‘Foliar and stem diseases of Eucalyptus in Vietnam and Thailand’. CSIRO Division of Forestry and ACIAR, Australia (internal report), Canberra. Palzer C (1978) Defoliation and death in Eucalyptus obliqua forest. Australian Forest Research Newsletter 5, 171. Park RF, Keane PJ, Wingfield MJ, Crous PW (2000). Fungal diseases of eucalypt foliage. In ‘Diseases and pathogens of eucalypts’. (Eds PJ Keane, GA Kile, FD Podger, BN Brown) pp. 153–239. (CSIRO Publishing: Melbourne) Parkin AM (1976) ‘The study of some aspects of leaf spots of Eucalyptus regnans F.Muell. and Eucalyptus obliqua L’Herit.’ Honours Thesis, School of Botany, La Trobe University, Australia. Pryor LD, Johnson LAS (1971) ‘A classification of the eucalypts.’ (Australian National University Press: Canberra) Purnell RC, Lindquist JE (1986) Provenance variation of Eucalyptus nitens on the Eastern Traansvaal Highveld in South Africa. South African Forestry Journal 138, 23–31. Sankaran KC, Sutton BC, Minter D (1995) ‘A checklist of fungi recorded from Eucalyptus.’ Mycological Papers 170 (Commonwealth Mycological Institute: Kew) SAS Institute Inc. (1992) ‘SAS Technical report P-229, SAS/STAT software: changes and enhancements. Release 6.09.’ (SAS Institute Inc.: Cary, NC) Spooner BM (1981) New records and species of British microfungi. Transactions of the British Mycological Society 76, 265–301. Stefanatos A (1993) ‘A study of the severity of leaf parasites of Eucalyptus globulus in a progeny trial and E. regnans in a silvicultural systems trial.’ Honours Thesis, School of Botany, La Trobe University, Australia. Stone C, Simpson JA, Eldridge RH (1998a) Insect and fungal damage to young Eucalypt plantings in northern New South Wales. Australian Forestry 61, 7–20. Stone C, Simpson JA, Gittens R (1998b) Differential impact of insect herbivores and their fungal pathogens on the Eucalyptus subgenera Symphyomyrtus and Monocalyptus and the genus Corymbia. Australian Journal of Botany 46, 723–734. Wall E, Keane PJ (1984) Leaf spot of Eucalyptus caused by Aulographina eucalypti. Transactions of the British Mycological Society 82, 257–273. Wilcox MD (1982a) Preliminary selection of suitable provenances of Eucalyptus regnans for New Zealand. New Zealand Journal of Forestry Science 12, 468–479. Wilcox MD (1982b) Selection of genetically superior Eucalyptus regnans using family tests. New Zealand Journal of Forestry Science 12, 480–493. Wingfield MJ, Crous PW, Peredo HL (1995) A preliminary, annotated list of foliar pathogens of Eucalyptus spp. in Chile. South African Forestry Journal 173, 53–57.

Received 30 October 2003, accepted 10 April 2003

400



Appendix I. Herbarium specimens Aulographina eucalypti (Cooke & Massee) Arx & Müller [anamorph: Thyrinula eucalypti (Cooke & Massee) H.J. Swart] on E. botryoides, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22873a); on E. brookeriana, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22874a); on E. cypellocarpa, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22875a); on E. elata, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22876a); on E. fraxinoides, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22877a); on E. globulus, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22878a); on E. grandis, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22879a); on E. nitens, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22880a); on E. oreades, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22881a); on E. quadrangulata, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22882a); on E. saligna, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22883a); on E. sieberi, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22884a); on E. smithii, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22885a); on E. viminalis, Tostaree, Nowa Nowa, East Gippsland, Vic., Feb. 1991, A.J. Carnegie (VPRI 22886a); on E. fastigata, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24891a); on E. muelleriana, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24893a); on E. dendromorpha, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24889a); on E. melliodora, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24892a); on E. cameronii, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24888a); on E. dunnii, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24890a); on E. badjensis, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24886a); on E. bosistoana, Darlimurla, South Gippsland, Vic., Dec. 1993, A.J. Carnegie (VPRI 24887a); on E. citriodora spp. variegata, Cavanaugh Plantation, Camira Creek, NSW, 17 Jan. 2002, A.J. Carnegie (DAR 76087); on E. cloeziana, Inglebar Plantation, Jackadgery, NSW, 14 March 2002, A.J. Carnegie (DAR 76088); on E. punctata, University of Western Sydney, Richmond, NSW, 15 Feb. 2002, A.J. Carnegie (DAR 76089); on E. haemastoma, University of Western Sydney, Richmond, NSW, 15 Feb. 2002, A.J. Carnegie (DAR 76090); on E. henryi, Inglebar Plantation, Jackadgery, NSW, 17 March 2002, A.J. Carnegie (DAR 76091); on E. transcontinentalis, Camberwell, Vic., 6 Nov. 1985, I.G. Pascoe (VPRI 12999a); on E. citridora, Mt. Gambier, S.A., Jan 1984, E. Wall, (VPRI 13237a); on E. cyanophylla, Canberra, ACT, 9 Feb. 1982, E. Wall, (VPRI 13244a); on E. leucoxylon, Mt. Gambier, South Australia, Jan. 1984, E. Wall (VPRI 13278a); on E. phaeotricha, Mt. Gambier, South Australia, Jan. 1984, E. Wall (VPRI 13310a); on E. polyanthemos, Nowa Nowa, Vic., 1983, R. Park (VPRI 13315a); on E. pyrocarpa, Mt. Gambier, South Australia, Jan. 1984, E. Wall (VPRI 13316a); on E. triflora, Canberra, ACT, 9 Feb. 1982, E. Wall (VPRI 13330a); on E. urnigera, Mt. Wellington, Tas., 1983, R. Park (VPRI 13335a); on E. ficifolia, Hill End, Vic., 8 Feb. 1986, I.G. Pascoe (VPRI 13365a); on E. rupicola, Montrose, Vic., 13 Feb 1986, I.G. Pascoe (VPRI 13474a); on E. tetraptera, Cheltenham, Vic., 1 July 1986, B.C. Sutton & I.G. Pascoe (VPRI 14039a); on E. grossa, Balwyn, Vic., 12 Aug 1986, I.G. Pascoe & B.C Sutton (VPRI 14182a); on E. stricklandii, Balwyn, Vic., 12 Aug 1986, B.C. Sutton & I.G. Pascoe (VPRI 14184a); on E. stricklandii, The Basin, Vic., 1 Mar 2000, B. Henderson (VPRI 22326a); on E. kitsoniana, The Basin, Vic., 25 Oct 2000, B. Henderson (VPRI 22567a); on E. gunnii, Silvan South, Vic., 20 Nov 2000, B. Rowe (VPRI 22641a); on E. platypus, Balwyn, Vic., 25 Jan 2002, V. Beilharz (VPRI 24927b); on E. cordifolia, Dural, NSW, 4 July 1964, L. Fraser (DAR 13952a); on E. eremophila, Bayview, NSW, 27 Oct. 1976, J. Walker (DAR 28265a); on E. lansdowneana, Helensburgh, NSW, 2 May 1982, P. Kable (DAR 42078a); on E. robusta, Baulkham Hills, NSW, 2 Sep. 1984, J. Walker (DAR 50116a); on E. stricta, Mount Werong, NSW, April 1962, W. Stahl (DAR 7088a); on E. torquata, Onooma, NSW, 12 Aug. 1976, W. Stahl (DAR 29600a).

Appendix II.

Recorded hosts of Aulographina eucalypti

Eucalyptus species

Eucalyptus subgenus (Brooker 2000)A

Country

Reference(s)

E. agglomerata

Eucalyptus

Australia

E. amplifolia E. andrewsii E. approximans E. badjensis E. baxteri E. bosistoana E. botryoides

Symphyomyrtus Eucalyptus Eucalyptus Symphyomyrtus Eucalyptus Symphyomyrtus Symphyomyrtus

E. bridgesiana E. brookeriana E. caesia E. camaldulensis

Symphyomyrtus Symphyomyrtus Symphyomyrtus Symphyomyrtus

E. cameronii E. citriodora E. citriodora spp. variegata E. cladocalyx E. cloeziana E. coccifera

Eucalyptus Corymbia Corymbia Symphyomyrtus Idiogenes Eucalyptus

Australia South Africa Australia Australia Australia Australia Australia New Zealand Australia Australia Australia Australia Vietnam Australia Australia Australia Australia Australia UK

Gerrettson-Cornell and Dowden (1977) Stone et al. (1998a) Crous et al. (1989) Wall and Keane (1984) B

Wall and Keane (1984) B

Marks et al. (1982), B M. Dick pers. comm.C Wall and Keane (1984) B

Wall and Keane (1984) Wall and Keane (1984) Old and Yuan (1994) B B B

Wall and Keane (1984) Carnegie 2000, B Spooner (1981)



Appendix II.

(Continued)

Eucalyptus species


Country

Reference(s)

E. consideniana E. cordata E. cordifolia E. cosmophylla E. costata E. cyanophylla E. cypellocarpa E. dalrympleana

Eucalyptus Symphyomyrtus Angophora Symphyomyrtus Angophora Symphyomyrtus Symphyomyrtus Symphyomyrtus

Wall and Keane (1984) Barber et al. (2003)

E. delegatensis

Eucalyptus

E. dendromorpha

Eucalyptus

E. diversicolor E. dives E. dunnii E. elata

Symphyomyrtus Eucalyptus Symphyomyrtus Eucalyptus

Australia Australia Australia Australia Australia Australia Australia Australia South Africa Australia New Zealand South Africa Australia New Zealand New Zealand Australia Australia South Africa Australia Australia New Zealand South Africa Australia Australia New Zealand New Zealand South Africa Australia Australia South Africa Australia USA South Africa Chile Australia New Zealand Australia Australia Australia Australia Australia Australia Australia Australia Australia Australia Australia South Africa Australia Australia Australia Australia Australia South Africa South Africa Australia New Zealand

E. eremophila E. fastigata

Symphyomyrtus Eucalyptus

E. ficifolia

Corymbia

E. fraxinoides

Eucalyptus

E. globoidea

Eucalyptus

E. globulus (includes 4 subsp.)

Symphyomyrtus

E. grandis

Symphyomyrtus

E. gregsoniana E. grossa E. gunnii E. haemastoma E. henryi E. johnstonii E. kitsoniana E. laevopinea E. lansdowneana E. lehmannii E. leucoxylon E. macarthurii E. macrorrhyncha E. maculata E. marginata E. melliodora E. microcorys E. moluccana E. muelleriana

Eucalyptus Symphyomyrtus Symphyomyrtus Eucalyptus Corymbia Symphyomyrtus Symphyomyrtus Eucalyptus Symphyomyrtus Symphyomyrtus Symphyomyrtus Symphyomyrtus Eucalyptus Corymbia Eucalyptus Symphyomyrtus Alveolata Symphyomyrtus Eucalyptus

B

Hansford (1954) Wall and Keane (1984) B

Marks et al. (1982), B Wall and Keane (1984) Crous et al. (1989) Marks et al. (1982) Dick (1982) Crous et al. (1989) B

M. Dick pers. comm. M. Dick pers. comm. Burdon and Chilvers (1964) B

Crous et al. (1989) B B

Dick (1982) Crous and Wingfield (1991) Stone et al. (1998a) B

M. Dick pers. comm. Dick (1982) Crous and Wingfield (1991) Stone et al. (1998a), B Marks et al. (1982) Crous et al. (1989) Marks et al. (1982), B Wall and Keane (1984) Crous et al. (1989) Wingfield et al. (1995) Wall and Keane (1984), B M. Dick pers. comm. Wall and Keane (1984) B B B B


Stone et al. (1998a) B


Crous et al. (1989) Wall and Keane (1984) Marks et al. (1982) Hansford (1954) B

Marks et al. (1982) Crous et al. (1989) Crous et al. (1989) B

M. Dick pers. comm.

401

402



Appendix II.

(Continued)

Eucalyptus species


Country

Reference(s)

E. nitens

Symphyomyrtus

E. nitidia E. obliqua

Eucalyptus Eucalyptus

E. oreades

Eucalyptus

Marks et al. (1982), B Dick (1982) Crous et al. (1989) Wall and Keane (1984) Marks et al. (1982) Crous et al. (1989) M. Dick pers. comm. Crous et al. (1989)

E. pauciflora

Eucalyptus

E. perriniana E. phaeotricha E. pilularis

Symphyomyrtus Eucalyptus Eucalyptus

E. platypus E. polyanthemos E. punctata E. pyrocarpa E. quadrangulata

Symphyomyrtus Symphyomyrtus Symphyomyrtus Eucalyptus Symphyomyrtus

Australia New Zealand South Africa Australia Australia South Africa New Zealand South Africa Australia Australia New Zealand Australia Australia Australia South Africa New Zealand Australia Australia Australia Australia South Africa Australia Australia Australia New Zealand South Africa Australia South Africa Australia New Zealand USA South Africa Australia New Zealand Australia Australia Australia Australia Australia New Zealand Australia Australia Australia Australia Australia Australia Australia New Zealand Australia

E. radiata E. regnans

Eucalyptus Eucalyptus

E. resinifera

Symphyomyrtus

E. robusta

Symphyomyrtus

E. saligna

Symphyomyrtus

E. sieberi E. smithii E. stellulata E. stricklandii E. stricta E. tenuiramis E. tetragona E. tetraptera E. torquata E. transcontinentalis E. triflora E. urnigera E. viminalis

Eucalyptus Symphyomyrtus Eucalyptus Symphyomyrtus Eucalyptus Eucalyptus Eudesmia Symphyomyrtus Symphyomyrtus Symphyomyrtus Eucalyptus Symphyomyrtus Symphyomyrtus

E. woodwardii

Symphyomyrtus

A

B

Burdon and Chilvers (1964) M. Dick pers. comm. Wall and Keane (1984) B

Marks et al. (1982) Crous et al. (1989) M. Dick pers. comm. B B B B

Crous et al. (1989) B

Burdon and Chilvers (1964) Marks et al. (1982) Dick (1982) Crous et al. (1989) Marks et al. (1982) Crous et al. (1989) B

M. Dick pers. comm. Wall and Keane (1984) Crous et al. (1989) B

M. Dick pers. comm. Marks et al. (1982), B B

Wall and Keane (1984) B B

M. Dick pers. comm. Wall and Keane (1984) B B B B B

Marks et al. (1982), B M. Dick pers. comm. Wall and Keane (1984)

The classification of genus Eucalyptus here follows Brooker (2000), and includes subgenus Corymbia (formerly a genus, Hill and Johnson 1995), subgenus Eucalyptus (formerly subgenus Monocalyptus, Pryor and Johnson 1971) and subgenus Angophora (formerly a genus, Pryor and Johnson 1971). B Recorded in present study. C Dr Margaret Dick, Forest Research, New Zealand.

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