Determining the temporal interaction of Camellia cultivar flowering periods and camellia petal blight disease presence in Auckland, New Zealand

Botanic gardens hold diverse and valuable living collections that provide a number of research, conservation and education opportunities. Auckland Botanic Gardens (ABG) has an internationally significant collection of species and cultivar camellias that have been used for scientific research into understanding which species are susceptible to camellia petal blight. ABG has surveyed all cultivars and species in its collection over multiple years to identify which camellias are affected by petal blight and which avoid it, based on their flowering period. A total of 363 camellias were assessed for petal blight over 6 years of surveying. It was found that 245 cultivars and 6 species were susceptible to the disease, while 68 cultivars and 32 species did not display any visual symptoms. These are important findings, as enthusiasts and breeders alike may use them to inform their respective interests. 1 Emma Bodley is Botanical Records and Conservation Specialist at Auckland Botanic Gardens. Address: 102 Hill Road, Manurewa, Auckland, New Zealand. Email: emma.bodley@aucklandcouncil.govt.nz 2 Rebecca Stanley is a Curator at Auckland Botanic Gardens. Address: as above. Introduction Botanic gardens play a key role in supporting and facilitating research. They hold diverse and important plant collections that provide researchers with convenient access to plants which are well documented on databases. Horticultural and botanical experts are available to make daily observations on growth, maintenance, and pests and diseases. Information that staff acquire through regular observations is captured on the databases; this provides an important life history of the plants, revealing information about them over time, such as their susceptibility to pests or diseases. Camellias have been grown in New Zealand as a common garden plant for decades. They provide autumn and winter interest in gardens as specimen trees and are also used as hedging (Fig. 1). They attract insect pollinators and birds to gardens at a time of year when there are fewer flowers around for foraging. Since the introduction to New Zealand in the early 1990s of the fungus Ciborinia camelliae, the causal agent of camellia petal blight, many Camellia cultivars have no longer been useful amenity plants because this disease infects the blooms, causing them to turn brown and fall early (Fig. 2). The fungus can be confirmed by removing a flower from the plant and looking on the back side for a grey ring of fungal hyphae at the base of the petals (Fig. 3). C. camelliae only infects the floral parts of a plant and is not known to infect any other genera 296.indd 1 19/11/2020 10:26 2 | Emma Bodley & Rebecca Stanley DOI 10.24823/Sibbaldia.2020.296 Fig. 1 Camellias are commonly used as hedging in New Zealand. Photo: Rebecca Stanley. Fig. 2 Brown flowers of Camellia japonica ‘Kate Sheppard’. Photo: Rebecca Stanley. 296.indd 2 19/11/2020 10:26 Temporal interaction of Camellia cultivar flowering periods and petal blight disease presence | 3 DOI 10.24823/Sibbaldia.2020.296 (Taylor & Long, 2000). Since as far back as 1919, C. camelliae has been found in other countries, including Japan, France, England, Spain, Italy, Germany, Switzerland, Portugal and the United States, but it did not become widespread until the 1970s (Taylor & Long, 2000). In the late 1990s, a survey undertaken throughout New Zealand found it to be widespread and likely to be dispersed by wind and the transfer of infected material (Taylor, 1999). Ciborinia camelliae is a host-specialist pathogen that only affects plants in the genus Camellia. Apothecia develop on sclerotia in spring and are dispersed by wind. These ascospores infect camellia petals quickly, causing the flowers to fall from the plant onto the ground (Taylor & Long, 2000). When the flowers are on the ground, the sclerotia develop on the petals and overwinter on the rotting flowers (Taylor & Long, 2000) until environmental conditions are suitable for starting the cycle of infection again. This means the fungus does not require a second species to complete its reproductive cycle. There are no strategies that prevent or control the annual reincursion of this fungus despite testing in various stages of the Ciborinia camelliae lifecycle with fungicides (Couselo et al., 2014). The disease affects larger-flowered, spring-blooming cultivars (japonica types) more frequently, partly because they flower later when the fungus is more active. The fungus is most active after a period of cool temperature followed by warming temperatures and moisture (American Camellia Society, 2020). However, spores can remain dormant for approximately four years until favourable conditions are met (Taylor, 2004). The disease is also more visible on larger and palerflowered blooms. Auckland Botanic Gardens (ABG) has had a significant collection of Camellia species and cultivars – a total of 521 varieties since the gardens opened in 1982 (Fig. 4). The collection was planted in 1985 with the help of the late Neville Haydon, the former owner of Camellia Haven nursery. There are few studies of camellia petal blight’s impact in gardens; however, some work has gone into testing a range of 39 Camellia for petal blight resistance. These range from C. pitardii × japonica ‘Nicky Crisp’ (Fig. 5), which has no resistance to the fungus, to C. lutchuensis (Fig. 6), which has high resistance (Denton-Giles et al., 2013). A breeding programme at ABG applies the knowledge from genetic work carried out by Denton-Giles et al. (2013) to select larger-flowered cultivars resistant to petal blight. The aim of this breeding programme is to develop a beautiful, Fig. 3 Grey ring on mould around the base of a Camellia japonica ‘Kate Sheppard’ flower. Photo: Rebecca Stanley. 296.indd 3 19/11/2020 10:26 4 | Emma Bodley & Rebecca Stanley DOI 10.24823/Sibbaldia.2020.296 Fig. 4 Auckland Botanic Gardens’ Camellia Garden contains a range of species and cultivars. Photo: Emma Bodley.


Introduction
Botanic gardens play a key role in supporting and facilitating research. They hold diverse and important plant collections that provide researchers with convenient access to plants which are well documented on databases. Horticultural and botanical experts are available to make daily observations on growth, maintenance, and pests and diseases. Information that staff acquire through regular observations is captured on the databases; this provides an important life history of the plants, revealing information about them over time, such as their susceptibility to pests or diseases.
Camellias have been grown in New Zealand as a common garden plant for decades. They provide autumn and winter interest in gardens as specimen trees and are also used as hedging (Fig. 1). They attract insect pollinators and birds to gardens at a time of year when there are fewer flowers around for foraging.
Since the introduction to New Zealand in the early 1990s of the fungus Ciborinia camelliae, the causal agent of camellia petal blight, many Camellia cultivars have no longer been useful amenity plants because this disease infects the blooms, causing them to turn brown and fall early (Fig. 2). The fungus can be confirmed by removing a flower from the plant and looking on the back side for a grey ring of fungal hyphae at the base of the petals (Fig. 3). C. camelliae only infects the floral parts of a plant and is not known to infect any other genera    , 2000). In the late 1990s, a survey undertaken throughout New Zealand found it to be widespread and likely to be dispersed by wind and the transfer of infected material (Taylor, 1999). Ciborinia camelliae is a host-specialist pathogen that only affects plants in the genus Camellia. Apothecia develop on sclerotia in spring and are dispersed by wind. These ascospores infect camellia petals quickly, causing the flowers to fall from the plant onto the ground (Taylor & Long, 2000). When the flowers are on the ground, the sclerotia develop on the petals and overwinter on the rotting flowers (Taylor & Long, 2000) until environmental conditions are suitable for starting the cycle of infection again. This means the fungus does not require a second species to complete its reproductive cycle.
There are no strategies that prevent or control the annual reincursion of this fungus despite testing in various stages of the Ciborinia camelliae lifecycle with fungicides (Couselo et al., 2014). The disease affects larger-flowered, spring-blooming cultivars (japonica types) more frequently, partly because they flower later when the fungus is more active. The fungus is most active after a period of cool temperature followed by warming temperatures and moisture (American Camellia Society, 2020). However, spores can remain dormant for approximately four years until favourable conditions are met (Taylor, 2004). The disease is also more visible on larger and palerflowered blooms.
Auckland Botanic Gardens (ABG) has had a significant collection of Camellia species and cultivars -a total of 521 varieties since the gardens opened in 1982 (Fig. 4). The collection was planted in 1985 with the help of the late Neville Haydon, the former owner of Camellia Haven nursery. There are few studies of camellia petal blight's impact in gardens; however, some work has gone into testing a range of 39 Camellia for petal blight resistance. These range from C. pitardii × japonica 'Nicky Crisp' (Fig. 5), which has no resistance to the fungus, to C. lutchuensis (Fig. 6), which has high resistance (Denton-Giles et al., 2013). A breeding programme at ABG applies the knowledge from genetic work carried out by Denton-Giles et al. (2013) to select larger-flowered cultivars resistant to petal blight. The aim of this breeding programme is to develop a beautiful,  petal blight during the initial assessment, cultivars were reassessed later in the flowering season. Detailed phenology records were not recorded during these surveys. Notes on phenology were, however, made on specific cultivars to help inform when to recheck flowers for petal blight.

Results
From the multiple surveys, we compiled a list of 245 cultivars which are susceptible to petal blight (  (Fig. 6). Although only the presence or absence of petal blight was recorded, we noted that some cultivars displayed symptoms differently. Dark-coloured flowers are less impacted aesthetically by petal blight because the brown petals are not as obvious in comparison to lighter flower colours. White and light pink flowers are aesthetically less attractive when infected with petal blight because the contrast between the light petals and the brown rot is greater.  Photo: Jack Hobbs.

Conclusion
There are at least ten cultivars where susceptibility is unclear from field observations because flowering times have not been recorded; these will be confirmed in subsequent years (Appendix). This requires not only observing the presence or absence of petal blight, but also recording phenology to gain an understanding of whether resistance or avoidance is the mechanism for the lack of petal blight. Although camellias are not commonly grown by gardeners, we have compiled a list of Camellia species and our observations of the impact on them of petal blight (Table 3). Until there is more success in breeding for resistance to camellia petal blight, we recommend that gardeners choose autumnflowering (sasanqua type) cultivars (Table 2) to avoid the unsightly effects of the disease. However, there are some late-flowering camellias that display no visual symptoms of petal blight which could be a result of their parentage providing some resistance (Table  4). These Camellia cultivars flower before Ciborinia camelliae releases its spores but some also have a certain resistance thanks to their parentage.
We provide an extensive list of petal blight free camellias and are happy to share this information with gardens, nurseries and other breeders. At ABG, we have gradually removed plants that have petal blight and so when people visit our garden, they will see healthy, petal blight free plants which will provide them with inspiration for planting at home. At ABG, we display plants that grow well in Auckland conditions, are free from pests or diseases and have spectacular flowering. We hope that this will help gardeners make choices about which cultivars to avoid planting and, in addition, will inform the ABG cultivar breeding programme with regard to the selection of resistant parents.