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Sorting out Gymnosporangium species – the aecial stage
Field Mycology Volume 7(4), October 2006
SORTING OUT GYMNOSPORANGIUM SPECIES = The aecial stage . Bert and Gill Brand* and Richard Shattock** ** * 14 Bishopton Lane, Stratford-on-Avon, Warwickshire CV37 9JN and 6Victoria Avenue, Bangor, Gwynedd LL57 2EP, UK
T
he four species of the rust genus Gymnosporangium which are established in Britain have been known here since before 1888 when Plowright described them in his book British Uredineae and Ustilagineae, using dried specimens from Berkeley, Cooke andVize. T h e life cycles of all species alternate between rosaceous trees and shrubs, on which the aecial stage grows, and Juniperus spp. which are hosts of the telial stage (Brand & Brand, 2001; 2004). In Britain the hosts Sorbus, Pyrus, Mespilus and Cydonia each only support mature aecial infections of a single Gymnosporangium species (Fig.1). Moreover, the aecia of G. sabinae and G. cornutum are distinctive under a hand lens, being barrel-shaped with a persistent cap in the former (Fig. 2) and cylindrical 3-5 mm long in the latter. On the other hand, both G. clavariiforme and G. confusum occur on Crataegus and the aecia look similar. Wilson & Henderson (1966) describe the tubular aecia of G. clavariiforme as shorter and wider (0.7-1.5 x 0.3-0.5 mm) than those of G. confusum (up to 4 x 0.1-0.3 mm). However, when the aecia mature the peridium rapidly splits and fragments starting near the outer end (Fig. 3 ) , so that the length character is soon lost. These authors also report that peridial cells can be longer in G. clavariiforme (70-130 pm) than in G. confusum (60-95 pm) but these ranges overlap considerably and at present we have insufficient evidence to establish the value of this character. T h e most useful distinguishing character is the type of ornamentation on certain walls of the peridial cells. T h e problem in using this character is that the
ornamentation differs on different faces of the peridial cells. T h e scanning electron microscope (SEM) shows up these differences. In both species the faces to the outside of the tubular aecia are smooth (Figs. 4 & 6) and the inner faces are somewhat papillate (Figs. 5 & 7), but the side walls between adjacent peridial cells are different in the two species. In G. clavariiforme the side walls have irregular papillae (arrowed in Figs. 4 & 5) whereas in G. confusum they have elongate warts and ridges which are obliquely arranged (arrowed in Fig. 7 and enlarged in Fig. 9). T h e ridges between adjacent cells seem to interlock, making them difficult to separate. When the peridial cells dry out the outer, smooth and thinner wall tends to collapse concavely, as can be seen in the SEM of the aecia of G. sabinae on pear (with papillate side walls, Fig. 8). Once these differences between different faces of the peridial cells are understood from these SEM images, the distinction between papillae and elongate warts and ridges can be seen under the light microscope when mounted in water. Patience is required to pull apart the peridial cells and mount them so that the ornamentation on the side walls can be seen in surface view. Distribution in Britain There is no well-documented evidence that the aecial stages can persist perennially. The aeciospores which are produced on these hosts can only infect junipers. The infections on junipers, however, are perennial on stems and, during wet weather in spring, produce teliospores which then produce basidiospores
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Field Mycology Volume 7(4), October 2006 which are the source of infection of the rosaceous hosts . The hosts of all these rusts are widely distributed in Britain (although varying in abundance) either as native, naturalised or garden plants. Crataegus and Sorbus occur in all vice counties and pear is very widely grown. The telial host Juniperus cornrnunis occurs as a wild plant mainly in Scotland, NW England and on the chalk downlands of SE England but there are numerous cultivars widely grown in gardens. The other group of telial hosts, mainly J. sabina, J. chinensis and their hybrids, are all introduced in Britain, but J. sabina has been grown here for at least 450 years. Cultivars with a prostrate bushy growth form have been popular in recent years. The distribution of G. cornuturn on Sorbus is the best documented of these rusts with 86 post-1985 entries in the BMSFRD. In the last twenty years all records are from the north of England (VCs 64, 65, 66, 67, 68, 70) and the Scottish highlands (88,89,91,92,93,95,96,98,105,106,107), with single records from Orkney and Ireland. Records of the other distinctive species, G. sabinae on Pyrus, are mainly from SE England. This species is poorly represented on the BMSFRD with only 10 post-1985 records (6 from Surrey, 2 from Warwicks and one each from W. Sussex and Herts), perhaps because pear is a cultivated plant. The Royal Horticultural Society,Wisley, Surrey receives enquiries about pear rust from RHS members. Although the distribution of these is biased towards members living close to Wisley, they have records from as far north as Cheshire. The RHS reports that pear rust has been more common and widespread in the last few years. The conclusion that it occurs in the midland area as well as the south-east is supported by seeing it in Warwickshire every year since 2003 and by the records and/or specimens sent to us in the last three years from Beds., Bucks., S.Hants., Herts., W. Gloucs., Surrey, and even from a young pear tree in SWYorkshire in 2004.
Establishing the distribution of the two species on Crataegus is complicated by their morphological similarity and the assumption, based on 1966 evidence (Wilson & Henderson, 1966), that G. clavariiforrne is the commoner and therefore the expected species. There are 19 post-1985 entries for G. clavariiforrne on Crataegus on the BMSFRD. Strikingly they are very widely scattered from E.Sutherland to S Devon and SE Galway to E Norfolk (Fig. lo). Of the recent specimens on Crataegus in England and Wales which we have seen or been told about only six have the peridial cell character of G. clavariiforrne, one each from Bucks., Herefs., Warks., Shropshire, Rads. and Durham. During August 2005 this species was found on Crataegus at 4 sites in the Cairngorms (VC 96, Easterness). In the Scottish Highlands Crataegus is not a common hedgerow plant and all the records were on planted Crataegus, on specimen trees of ornamental cultivars at three of the sites. Post-1985 records of G. confusurn (Fig. 11) are heavily biased by our local efforts in Warwickshire where Crataegus is the commonest hedgerow plant. However, 2004 was a good year for infection of Crataegus and with the help of correspondents over recent years the range of G. confusurn has been extended into all adjacent vice counties, in the wes; as far as Shropshire and Herefs. and in the south as far as W. Gloucs., N. Wilts., and Berks. The confirmation of G. confusurn on Crataegus in Bangor Faerns.) in 2005 and a 1988 report from E. Norfolk open up the possibility of a much wider distribution. The only area in which evidence is accumulating that the fungus is absent (or rare) is to the east beyond the western borders of vice counties Leics. and Northants., where several interested rust watchers have failed to find it. Recent records of this rust on Mespilus and Cydonia are also from the western midlands. Wilson & Henderson (1966) describe G. confusurn and G. sabinae as scarce. This is no longer the case. It seems that these species have become more widespread and more
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Field Mycology Volume 7(4), October 2006 frequent, at least in some recent years. More information about the occurrence of aecial stages (based on microscopic examination for the two species on Crataegus) and also the telial stages is needed to understand their current distribution and to reveal any changes which may be occurring. Please tell us about finds!
Acknowledgements We thank Alison Bell, School of Biological Sciences, University of Wales, Bangor, for electron microscopy; Chris Prior, James Armitage, Ian Waghorn, Beatrice Henricot and Caroline Gorton at the R H S, Wisley for information, especially about pear rust; and numerous fellow rust watchers for their interest, observations and specimens.
References Brand, A.W. & Brand, G.M. (200 1). Have you seen this? AWanvickshire oddity. Field Mycology, 2: 66-67. Brand, A.W. & Brand, G.M. (2004).The other half. The telial stage of the rust fungus Gyrnnosporangiurnconfusum. Field Mycology, 5 : 14- 16. Wilson, M. & Henderson, D.M. (1966). British Rust Fungi. Cambridge, UK: Cambridge University Press. Footnote Analysis of BMSFRD records for this article was completed at the end of 2005. New records are continually being added to the database.
Fig.
Aecial host Fig.1. Telial and aecial hosts of different species of Gymnosporangium in Britain. Figs. 2&3. Scanning electron microscopy of the aecia of Gymnosporangium sabinae on Pyrus (2) and G. confusum on Crataegus (3). Magnification x35. Figs. 4-8. Scanning electron microscopy of the aecial peridium. Outer (4) and inner (5) faces in G. clavariiforme on Crataegus and outer(6) and inner (7) faces in G. confusum on Mespilus and collapsed cells of the fragmented peridium (8) in G. sabinae on Pyrus. The different ornamentation on the side walls of the cells can be seen where the peridium has split (arrowed, papillae in G. clavariiforme (4 &5) and G. sabinae. (8) and diagonal ridges in G. confusum (7)). Magnification x 900. Fig. 9. The arrowed portion of Fig. 7 enlarged to show the diagonal ridges on the side wall of a peridial cell in G. confusum. Magnification x2800.
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Field Mycology Volume 7(4), October 2006
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Field Mycology Volume 7(4), October 2006
Figs. 10 &11. Post -1985 distribution by Vice County of aecia of G. clavariiforme (10) and G.confusum (11) on Crataegus, based on BMSFRD records together with personal records and specimens and information from correspondents. The authors have seen specimens of G. confusum from all recorded vice counties except East Norfolk (27). For G. clavariiformewe have seen specimens from only four vice counties (Bucks 24, Warwicks 38, Shropshire 40 and Easterness 96).
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SORTING OUT GYMNOSPORANGIUM SPECIES = The aecial stage . Bert and Gill Brand* and Richard Shattock** ** * 14 Bishopton Lane, Stratford-on-Avon, Warwickshire CV37 9JN and 6Victoria Avenue, Bangor, Gwynedd LL57 2EP, UK
T
he four species of the rust genus Gymnosporangium which are established in Britain have been known here since before 1888 when Plowright described them in his book British Uredineae and Ustilagineae, using dried specimens from Berkeley, Cooke andVize. T h e life cycles of all species alternate between rosaceous trees and shrubs, on which the aecial stage grows, and Juniperus spp. which are hosts of the telial stage (Brand & Brand, 2001; 2004). In Britain the hosts Sorbus, Pyrus, Mespilus and Cydonia each only support mature aecial infections of a single Gymnosporangium species (Fig.1). Moreover, the aecia of G. sabinae and G. cornutum are distinctive under a hand lens, being barrel-shaped with a persistent cap in the former (Fig. 2) and cylindrical 3-5 mm long in the latter. On the other hand, both G. clavariiforme and G. confusum occur on Crataegus and the aecia look similar. Wilson & Henderson (1966) describe the tubular aecia of G. clavariiforme as shorter and wider (0.7-1.5 x 0.3-0.5 mm) than those of G. confusum (up to 4 x 0.1-0.3 mm). However, when the aecia mature the peridium rapidly splits and fragments starting near the outer end (Fig. 3 ) , so that the length character is soon lost. These authors also report that peridial cells can be longer in G. clavariiforme (70-130 pm) than in G. confusum (60-95 pm) but these ranges overlap considerably and at present we have insufficient evidence to establish the value of this character. T h e most useful distinguishing character is the type of ornamentation on certain walls of the peridial cells. T h e problem in using this character is that the
ornamentation differs on different faces of the peridial cells. T h e scanning electron microscope (SEM) shows up these differences. In both species the faces to the outside of the tubular aecia are smooth (Figs. 4 & 6) and the inner faces are somewhat papillate (Figs. 5 & 7), but the side walls between adjacent peridial cells are different in the two species. In G. clavariiforme the side walls have irregular papillae (arrowed in Figs. 4 & 5) whereas in G. confusum they have elongate warts and ridges which are obliquely arranged (arrowed in Fig. 7 and enlarged in Fig. 9). T h e ridges between adjacent cells seem to interlock, making them difficult to separate. When the peridial cells dry out the outer, smooth and thinner wall tends to collapse concavely, as can be seen in the SEM of the aecia of G. sabinae on pear (with papillate side walls, Fig. 8). Once these differences between different faces of the peridial cells are understood from these SEM images, the distinction between papillae and elongate warts and ridges can be seen under the light microscope when mounted in water. Patience is required to pull apart the peridial cells and mount them so that the ornamentation on the side walls can be seen in surface view. Distribution in Britain There is no well-documented evidence that the aecial stages can persist perennially. The aeciospores which are produced on these hosts can only infect junipers. The infections on junipers, however, are perennial on stems and, during wet weather in spring, produce teliospores which then produce basidiospores
123
Field Mycology Volume 7(4), October 2006 which are the source of infection of the rosaceous hosts . The hosts of all these rusts are widely distributed in Britain (although varying in abundance) either as native, naturalised or garden plants. Crataegus and Sorbus occur in all vice counties and pear is very widely grown. The telial host Juniperus cornrnunis occurs as a wild plant mainly in Scotland, NW England and on the chalk downlands of SE England but there are numerous cultivars widely grown in gardens. The other group of telial hosts, mainly J. sabina, J. chinensis and their hybrids, are all introduced in Britain, but J. sabina has been grown here for at least 450 years. Cultivars with a prostrate bushy growth form have been popular in recent years. The distribution of G. cornuturn on Sorbus is the best documented of these rusts with 86 post-1985 entries in the BMSFRD. In the last twenty years all records are from the north of England (VCs 64, 65, 66, 67, 68, 70) and the Scottish highlands (88,89,91,92,93,95,96,98,105,106,107), with single records from Orkney and Ireland. Records of the other distinctive species, G. sabinae on Pyrus, are mainly from SE England. This species is poorly represented on the BMSFRD with only 10 post-1985 records (6 from Surrey, 2 from Warwicks and one each from W. Sussex and Herts), perhaps because pear is a cultivated plant. The Royal Horticultural Society,Wisley, Surrey receives enquiries about pear rust from RHS members. Although the distribution of these is biased towards members living close to Wisley, they have records from as far north as Cheshire. The RHS reports that pear rust has been more common and widespread in the last few years. The conclusion that it occurs in the midland area as well as the south-east is supported by seeing it in Warwickshire every year since 2003 and by the records and/or specimens sent to us in the last three years from Beds., Bucks., S.Hants., Herts., W. Gloucs., Surrey, and even from a young pear tree in SWYorkshire in 2004.
Establishing the distribution of the two species on Crataegus is complicated by their morphological similarity and the assumption, based on 1966 evidence (Wilson & Henderson, 1966), that G. clavariiforrne is the commoner and therefore the expected species. There are 19 post-1985 entries for G. clavariiforrne on Crataegus on the BMSFRD. Strikingly they are very widely scattered from E.Sutherland to S Devon and SE Galway to E Norfolk (Fig. lo). Of the recent specimens on Crataegus in England and Wales which we have seen or been told about only six have the peridial cell character of G. clavariiforrne, one each from Bucks., Herefs., Warks., Shropshire, Rads. and Durham. During August 2005 this species was found on Crataegus at 4 sites in the Cairngorms (VC 96, Easterness). In the Scottish Highlands Crataegus is not a common hedgerow plant and all the records were on planted Crataegus, on specimen trees of ornamental cultivars at three of the sites. Post-1985 records of G. confusurn (Fig. 11) are heavily biased by our local efforts in Warwickshire where Crataegus is the commonest hedgerow plant. However, 2004 was a good year for infection of Crataegus and with the help of correspondents over recent years the range of G. confusurn has been extended into all adjacent vice counties, in the wes; as far as Shropshire and Herefs. and in the south as far as W. Gloucs., N. Wilts., and Berks. The confirmation of G. confusurn on Crataegus in Bangor Faerns.) in 2005 and a 1988 report from E. Norfolk open up the possibility of a much wider distribution. The only area in which evidence is accumulating that the fungus is absent (or rare) is to the east beyond the western borders of vice counties Leics. and Northants., where several interested rust watchers have failed to find it. Recent records of this rust on Mespilus and Cydonia are also from the western midlands. Wilson & Henderson (1966) describe G. confusurn and G. sabinae as scarce. This is no longer the case. It seems that these species have become more widespread and more
124
Field Mycology Volume 7(4), October 2006 frequent, at least in some recent years. More information about the occurrence of aecial stages (based on microscopic examination for the two species on Crataegus) and also the telial stages is needed to understand their current distribution and to reveal any changes which may be occurring. Please tell us about finds!
Acknowledgements We thank Alison Bell, School of Biological Sciences, University of Wales, Bangor, for electron microscopy; Chris Prior, James Armitage, Ian Waghorn, Beatrice Henricot and Caroline Gorton at the R H S, Wisley for information, especially about pear rust; and numerous fellow rust watchers for their interest, observations and specimens.
References Brand, A.W. & Brand, G.M. (200 1). Have you seen this? AWanvickshire oddity. Field Mycology, 2: 66-67. Brand, A.W. & Brand, G.M. (2004).The other half. The telial stage of the rust fungus Gyrnnosporangiurnconfusum. Field Mycology, 5 : 14- 16. Wilson, M. & Henderson, D.M. (1966). British Rust Fungi. Cambridge, UK: Cambridge University Press. Footnote Analysis of BMSFRD records for this article was completed at the end of 2005. New records are continually being added to the database.
Fig.
Aecial host Fig.1. Telial and aecial hosts of different species of Gymnosporangium in Britain. Figs. 2&3. Scanning electron microscopy of the aecia of Gymnosporangium sabinae on Pyrus (2) and G. confusum on Crataegus (3). Magnification x35. Figs. 4-8. Scanning electron microscopy of the aecial peridium. Outer (4) and inner (5) faces in G. clavariiforme on Crataegus and outer(6) and inner (7) faces in G. confusum on Mespilus and collapsed cells of the fragmented peridium (8) in G. sabinae on Pyrus. The different ornamentation on the side walls of the cells can be seen where the peridium has split (arrowed, papillae in G. clavariiforme (4 &5) and G. sabinae. (8) and diagonal ridges in G. confusum (7)). Magnification x 900. Fig. 9. The arrowed portion of Fig. 7 enlarged to show the diagonal ridges on the side wall of a peridial cell in G. confusum. Magnification x2800.
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Field Mycology Volume 7(4), October 2006
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Field Mycology Volume 7(4), October 2006
Figs. 10 &11. Post -1985 distribution by Vice County of aecia of G. clavariiforme (10) and G.confusum (11) on Crataegus, based on BMSFRD records together with personal records and specimens and information from correspondents. The authors have seen specimens of G. confusum from all recorded vice counties except East Norfolk (27). For G. clavariiformewe have seen specimens from only four vice counties (Bucks 24, Warwicks 38, Shropshire 40 and Easterness 96).
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