Mar 25, 2012 - MaÃnahmen zur Verminderung der Verluste durch. Fruchtfäulnis beim Apfel. Mitt d OVR d Alten Landes 60, 46-52. Rizzoli W & Acler A, 2009.
Improving apple quality by hot water treatment PhD Thesis by Peter Maxin
Foreword This Ph.D. dissertation has been submitted to Aarhus University in partial fulfillment of the requirements of the degree Doctor of Philosophy. Dr. Hanne Lindhard Pederson (Associate Professor) was my primary supervisor until she left the University on 31 August 2011, at which time Dr. Michelle Williams (Head of Department) took on this responsibility. Dr. Roland Weber (Esteburg, Fruit Research and Advisory Centre, Jork; Germany) and Prof. Susan Lurie (Department of Food Science, Volcani Center, Israel) were co-supervisors. This study was conducted from 3 September 2008 to 9 December 2011 at the Department of Food Science, Aarhus University, located at Aarslev, Denmark. The study had a short-term interruption due to paternity leave for a total of 14 weeks. In February to March 2011, I stayed at the Esteburg Fruit Research and Advisory Center to carry out an ad hoc Ph.D. course. The primary focus of this Ph.D. project was apple fruit quality in relation to pre-storage hot-water treatments. The first year results showed neither an improvement nor any difference in physiological fruit quality following cold storage. Therefore, the main emphasis of the second and third project years was on fungal decay, the impact of hot water treatments, influences of pre-harvest factors on storage rot development and the introduction of a short term hot water treatment. Work on the latter aspect was initiated in October 2009 during a seven-day visit to the Volcani Center, Israel, where I worked with Professor Elazar Fallik. I am indebted to Roland Weber for his input and for the time we spend identifying the different fungi associated with storage rots. I also thank him for his contribution to PCR identification of the fungi which provided the opportunity to produce highimpact results. This thesis is presented in eight chapters. Chapter 1 is a general introduction on the Danish fruit growing sector and the connections to this study; Chapter 2 is a literature review on different fungi causing storage rots as well as commonly used chemical treatments and hot water treatments to reduce postharvest losses in apples. General methods that were used and developed in this Thesis are presented in Chapter 3. Chapter 4 contains a series of short trials that describe unpublished and preliminary results. It is the intention to repeat some of these findings for subsequent publication. i
Chapters 5 to 7 contain the results of key experimental work. In Chapter 8 key general results from this thesis are discussed, brief conclusions and a perspective for this technology are provided. References are contained in Chapter 9. I am very grateful for fruit donations generously made by Heinrich zum Felde (Jork), Alexander and Berbel Maxin (Jork), Peter Rolker (Jork), the Esteburg Centre and Michael Clever (Jork). This research needed a copious supply of plastic boxes, as used by many fruit farmers but not necessarily universities. I therefore extend my special thanks to Peter Rolker and to Bastian Benduhn (Esteburg Centre) for lending me the fruit storage boxes, and to Ørskov Frugt (Oure, Denmark) for shipping these boxes to Denmark and back to Germany. I also thank Berg GmbH and Jürgen Schacht (Jork) for their input of time and equipment in the first year trials on hot water rinsing. Carsten Sørensesn, Innotheque APS, Middelfart, Denmark generous provided time and initiative in developing and creating the prototype of a hot-water rinsing machine that could, after modifications, run the second year hot water rinsing experiments. Dr. Dirk Köpcke (Esteburg Centre) collaborated on both DCA and CA experiments, and stored hot water treated apples in his research facilities, therefore helping to clarify the behavior of pretreated fruit in these storage environments. I am very grateful to the technical staff at the Department of Food Science, Aarhus University, Aarslev, and especially to Annette and Stig Sørensen. A special “thank you” also goes to the secretarial staff for their smooth and efficient help with administrative matters. I am grateful for the support given to me by the Weber, Williams and Maxin families, and especially by my own family; Meike and Paul. This is in acknowledgement of the time my supervisors spent with me rather than their families, and of the time that I spent on the road instead of being at home. Thank you, Hanne, Michelle and Roland, for your critical advice in sharpening and polishing this Thesis and the various publications that form part of it. I thank my sister Uta Maxin for her input into improving the process figures in Chapter 4.
ii
Thanks are also given to all the colleagues at the Department of Food Science, Aarhus University for providing a collaborative, welcoming and positive study environment.
Thank you! Peter Maxin Aarslev; Denmark 25 March, 2012
This research was partially funded by the EU found ‘Isafruit’ (Project No. 016279), by the Danish Ministry of Food, Agriculture and Fisheries funded project ‘Bæredygtig fremtid for dansk konsumfrugt’ (J.nr: 3412-09-02385) and Plan Danmark funding.
iii
Table of contents Foreword ...................................................................................................................................................................... i Table of contents .................................................................................................................................................. iv Summary .................................................................................................................................................................. vii Resumé ...................................................................................................................................................................... ix Chapter 1: Introduction ...................................................................................................................................... 1 Chapter 2: Literature review .......................................................................................................................... 5 2.1 Scale of postharvest losses.................................................................................................................. 5 2.2 Incidence of storage-rot fungi........................................................................................................... 6 2.3 Postharvest fruit rots of apples ........................................................................................................ 10 2.4 Invasions of new fungi (neomycota) .......................................................................................... 22 2.5 Chemical control of storage rots................................................................................................... 24 2.6 Fungicides under pressure ............................................................................................................... 26 2.7 Control with heat, GRAS yeasts and hygiene ....................................................................... 28 2.8 Heat treatments...................................................................................................................................... 29 2.9 Apple Quality........................................................................................................................................... 32 Chapter 3: General methodology ............................................................................................................ 35 3.1 Introduction ............................................................................................................................................... 35 3.2 Example of the sequence of procedures of an entire experiment ............................ 35 3.3 Hot water dipping method............................................................................................................... 40 3.4 Hot water rinsing methods ............................................................................................................... 41 3.5 Identification of fungi .......................................................................................................................... 45 Chapter 4: Preliminary results ...................................................................................................................... 47 4.1 Pre-harvest effects on the development of storage rots ................................................. 47 4.2 Effects of HWT on fruit quality and physiology ..................................................................... 55 4.3 Effects of HWT on pathology .......................................................................................................... 73 Chapter 5: Paper 1 Hot-Water Dipping of Apples to Control Penicillium expansum, Neonectria galligena and Botrytis cinereaI: Effects of Temperature on Spore Germination and Fruit Rots ........................................................................................................................... 82 Summary ............................................................................................................................................................ 82 Introduction....................................................................................................................................................... 83 Materials and Methods ............................................................................................................................... 84 iv
Results .................................................................................................................................................................. 86 Discussion .......................................................................................................................................................... 91 Acknowledgements .................................................................................................................................... 95 References ........................................................................................................................................................ 96 Chapter 6: Paper 2 Control of Phacidiopycnis washingtonensis storage rot of apples by hot-water treatments but not by 1-MCP ...................................................................................... 100 Abstract ............................................................................................................................................................ 100 1
Introduction ........................................................................................................................................... 101
2
Materials and methods ................................................................................................................... 101
3
Results and discussion..................................................................................................................... 103
Acknowledgements ................................................................................................................................. 106 References ..................................................................................................................................................... 106 Chapter 7: Paper 3 Control of a wide range of storage rots in naturally infected apples by hot-water dipping and rinsing .......................................................................................... 108 Abstract ............................................................................................................................................................ 108 Keywords ........................................................................................................................................................ 109 1. Introduction............................................................................................................................................... 109 2. Materials and methods ...................................................................................................................... 110 3. Results .......................................................................................................................................................... 113 4. Discussion .................................................................................................................................................. 120 5. Conclusions .............................................................................................................................................. 122 Acknowledgements ................................................................................................................................. 123 References ..................................................................................................................................................... 123 Chapter 8: General Discussion................................................................................................................. 127 8.1 Hypotheses underlying this Thesis ............................................................................................ 127 8.2 Effects of delayed ripening on the incidence of storage rots .................................... 128 8.3 The influence of heat on spores and fruit ............................................................................. 131 8.4 Perspectives .......................................................................................................................................... 134 Chapter 9: Literature ...................................................................................................................................... 137
v
vi
Summary The Danish fruit industry has a focus on sustainable production systems. However, there is a need for new tools and technologies to enable orchardists to deliver quality fruit at competitive prices into the market. Research activities at Aarhus University aim to improve the availability and consumption of quality and healthy fruit. The use of postharvest hot-water treatments (HWT) can reduce storage losses of organically grown apples, as has been shown in several trials for different fungi. Preliminary results are presented as a follow up on different research activities in this Thesis. Seven short studies are aligned to three themes; pre harvest effect on the developing storage rots, effect of hot water treatments on fruit quality and physiology and effect of hot water treatments on pathology. The distribution of storage rot fungi in apples over two years was investigated in one orchard. The single-tree infection rate influenced by local inoculum and changing between years is reported. The influence of root pruning of different rootstocks on inoculum and decay rate in apples was investigated. The effect of crop load and nutrition level on fruit quality parameters (firmness, colour, sugar content, heat scald index) was also examined. Neither an improvement nor a quality decrease could be found following moderate hot water treatments. Hot water dipping (HWD) temperatures exceeding 54°C for 3 min resulted in severe heat scald. The influence of hot water rinsing (HWR), hot water dipping and 1-methycyclopropene (1-MCP) on the incidence of ‘Elstar’ skin spots under different atmosphere storage was evaluated. Evaporation of water through the fruit skin of HWR, HWD and cold water dipped control fruit was evaluated during a 36 h stress treatment. After 36 h, HWR treated fruit showed a trend towards a reduced loss of water through the cuticle relative to control fruit. The efficacy of HWD in limiting the further development of Sooty-blotch disease during storage was examined. Following HWD, Sooty-blotch fungi neither showed any further development in storage, nor was there any reduction in the existing mycelium. Hot water dipping (HWD) of spore suspensions of different storage rots was carried out to determine the effective temperature causing a 50% inhibition of spore viability (ET50) and the mortality curve in response to dipping temperature. Spore suspensions of Penicillium expansum, Neonectria galligena and Botrytis cinerea were used to inoculate apple fruit and to evaluate HWD efficacies in a wide range of vii
temperatures. Spores of P. expansum were inoculated both pre- and post-HWD. Similar developments of P. expansum rot in fruit inoculated pre- and post-HWD in the temperature range of 44-53°C led to a new perspective on the mode of action of HWD. An indirect effect of HWD as a heat-shock which induces the immune response of the fruit is contrasted with its direct inhibitory effect on fungal inoculum. A new storage rot, rubbery rot caused by the fungus Phacidiopycnis washingtonensis, was reported for the first time from Denmark. A description of the new rot, the orchard where it was detected and the incidence of decay were documented. The response of P. washingtonensis spores to HWD and the response of artificially inoculated fruit towards HWD were investigated. Naturally infected fruit with P. washingtonensis were subjected to HWD and HWR, and compared with fruit subjected to 1-MCP in both controlled atmosphere (CA) and dynamically controlled atmosphere (DCA) storage. The efficacies of HWD and HWR towards P. washingtonensis were comparable to Neofabraea spp. The influence of ripening inhibition caused by 1-MCP, CA or DCA did not influence the incidence of P. washingtonensis.. Combinations in time and temperature for rinsing and dipping of naturally infected apples in hot water were tested against natural infections of Neofabraea perenanns,
N. alba, N. galligena, B. cinerea, P. expansum, Monilinia fructigena, Colletrotricum acutatum, P. washingtonensis, Phoma exigua, Gibberella avenacea, Mucor spp. and Cladosporium spp. The influence of heat scald on the incidence of storage infections by P. expansum and a higher disease incidence by several pathogens following elevated temperatures were discussed. HWR showed comparable efficacies to HWD. Several advantages of HWR were discussed. The findings of this study are compared to previously reported and recent research results within the area of hot water dipping, fruit quality and fungal storage rots in apples. An overview on storage rots and postharvest control means is given in the context of organic farming. The general mode of action of HWT is evaluated for different fungi and apple varieties. Possible implementation strategies and perspectives of HWR for the apple industry are discussed.
viii
Resumé Den danske frugtbranche og Aarhus Universitet har i fællesskab sat fokus på bæredygtige produktionssystemer, som har til formål at forbedre adgangen til og forbruget af sund kvalitetsfrugt. I den forbindelse er der behov for at udvikle nye værktøjer og teknologier for at frugtavlerne kan producere kvalitetsfrugt til konkurrencedygtige priser. Brugen af varmtvands-behandlinger (HWT) efter høst er en sådan ny teknologi, som allerede har vist sig effektiv til bekæmpelse af flere forskellige rådsvampe i økologisk æbleproduktion. Der blev gennemført forsøg med neddypning af sporesuspensioner i varmtvand (HWD) og efterfølgende blev LD50 og mortalitetskurver for forskellige rådsvampe fastlagt i relation til vandets temperatur. Æbler blev podet med sporesuspensioner af Penicillium expansum, Neonectria galligena og Botrytis cinerea og effekten af HWD blev evalueret ved forskellige temperaturer. Sporer af P. expansum blev inokuleret både før og efter HWD (44-53° C) og efterfølgende sås en ensartet udvikling af P. expansum råd uafhængig af podningstidspunkt. Det førte til nye erkendelser omkring virkningsmekanismen bag HWD. Tidligere antog man HDW havde en direkte hæmmende effekt på svampesporerne, mens det nu forekommer sandsynligt, at der er tale om en indirekte virkning af HWD, hvor varmechokket inducerer en immunrespons i frugten. En ny lagersygdom forårsaget af svampen Phacidiopycnis washingtonensis, er fundet for første gang i Danmark. Symptomerne på sygdommen er en gummiagtig forrådnelse af hele frugten. Sygdommen er beskrevet og angrebsgraden og forekomsten i den plantage, hvor den blev fundet er dokumenteret. Virkningen af HDW på P. washingtonensis sporer og kunstig inokuleret frugt blev undersøgt. Naturligt inficeret frugt med P. washingtonensis blev udsat for HWD og varmtvandsoverbrusning (HWR), og sammenlignet med frugt der blev behandlet med SmartFresh (1-methylcyclopropen). Frugterne blev efterfølgende opbevaret under hhv. kontrolleret atmosfære (CA) og dynamisk kontrolleret atmosfære (DCA). Effekten af HWD og HWR mod P. washingtonensis var positiv og sammenlignelig med hvad der blev opnået overfor Neofabraea spp. Derimod havde SmartFresh, som
ix
hæmmer modningsprocesserne i frugten, ingen indflydelse på forekomsten af P. washingtonensis. Frugter der var naturligt inficeret med Neofabraea perenanns, N. alba, N. galligena, B. cinerea, P. expansum, Monilinia fructigena, Colletrotricum acutatum, P. washingtonensis , Phoma exigua, Gibberella avenacea, Mucor spp. og Cladosporium spp. blev dyppet eller overbruset med varmtvand i forskellige kombinationer af tid og temperatur. Ved både HWD og HWR kan for høje temperaturer forårsage skoldningsskader på frugten, som giver anledning til øgede angreb af P. expansum og andre patogener. HWR og HWD viste sammenlignelige virkningsgrader, og flere fordele ved HWR diskuteres. Yderligere resultater præsenteres mere kortfattet. Det blev undersøgt om HWD kunne begrænse den videre udvikling af sodplet under lagring, og der kunne ikke konstateres nyvækst af svampen på lageret, og eksisterende infektioner ikke kunne dræbes ved HWD. Forekomsten af lagersygdomme blev fulgt over 2 år i den samme plantage, og forskelle i infektionsgrader mellem træer og år blev beskrevet. Effekten af rodbeskæring på forekomsten af rådsvampe og tab under lagring blev undersøgt. Betydning af udbytteniveau og ernæringstilstand for forekomsten af skader efter HWD blev undersøgt. Det kunne konkluderes at moderat (og effektiv) HWD hverken forbedrede eller forringede frugtkvaliteten (fasthed, farve, sukkerindhold). HWD, hvor temperaturen overstiger 54° C i 3 minutter, resulterede i alvorlige skoldningsskader. Det blev undersøgt om frugterne mistede spændstighed (fordampning gennem frugtskrællen) efter behandling med HWD og HWR. Efter 36 timers varmestress tenderede de HWR behandlede frugter til at have mistet mindre vand end frugter som var behandlet med HWD eller kontrol frugter, som var dyppet i koldt vand. Resultaterne i denne afhandling er sammenlignet med tidligere publicerede forskningsresultater inden for området af varmtvandsbehandling, frugtkvalitet og lagersygdomme i æbler. Der gives en oversigt over lagersygdomme og mulige kontrolforanstaltninger indenfor en kontekst af økologisk frugtavl. Den overordnede virkningsmekanisme af HWT vurderes på forskellige svampe og æblesorter. Mulighederne for implementering og fremtidige strategier for HWR til brug i æbleindustrien diskuteres. x
Chapter 1: Introduction The fruit industry in Denmark is challenged by global competitors. Denmark’s economy is one of the strongest in the world in terms of per capita income (Einhorn and Logue 2010) and, therefore, it is an attractive market for all types of highly priced food products. Despite this competition in the market place, Danish apples are sold at high prices in the supermarkets. However, relatively little revenue is returned to Danish orchardists; in the years 2009 (reflecting the season 2008/9), 2010 and 2011 the average payment to growers was 2.75 DKK (=0.21€) per kg apples (pers. communication Ejvin Straaup, Langeland, DK). This return to the growers did not cover the production costs in established orchards, which were equivalent to 3 DKK (=0.23€) per kg apples (Pedersen 2006). Danish regulations currently disadvantage Danish orchardists in the market place. Danish growers must meet tight Danish regulations and yet they compete on their own market with imported fruit produced under different environmental and social requirements. For example, in 2009 the only registered active compounds for organically managed Danish orchards were wettable sulphur and Bacillus thuringiensis, whereas a comparable orchardist in Germany would have had access to more than 20 registered compounds (based on Annex II of the organic EU directive 2092/91 from 1991, subsequently replaced by EU directive 834/2007). In addition, production costs in Denmark are comparatively high as a result of high salary costs and taxation on pesticides and fertilizers. Previously, a reasonable income for orchardists in the years 2002 to 2005 (ca. 4-5 DKK/kg) led to enhanced planting activities in 2005 as well as 2006, thereby increasing the apple growing area. In Denmark 1,267 ha apples were cultivated in 2005, increasing to 1,609 ha in 2010. These numbers include organic apple orchards which increased from 158 ha in 2005 to 300 ha in 2010. To limit overhead in growers’ organizations (GO) and to reduce sales competition, restructuring and merging of some GO started in 2008 and has not yet been completed in 2012. The annual Danish apple season starts with the summer apple ‘Transparente’ which is harvested at the end of July in average years. Due to climate limitations, ‘Golden Delicious’ marks the latest possible variety with an approximate harvest time from 1
Chapter 1: Introduction
mid-October until early November. The average Danish apple consumption is 15 kg fresh apple per person per annum. The local production has a market share of 30%, the remaining demands being met by imports (Danmarks Statistik 2007). Danish fruits are marketed until March (Dansk Kernefrugt, 2011).
Figure 1.1: Variety spectrum of Danish apple production (1,486 ha in total) for the year 2007. Varieties grown on less than 20 ha (30% of the days having rainfall and an average temperature of 11-16°C for more than 8 h per day (Beresford and Kim 2011). Sporulation, spore dispersal and infections of N.
galligena are directly linked with rainfall (McCracken et al. 2003). Fruit infections by N. galligena can be categorized into two groups, i.e. eye rot (blossom-end rot) and lenticel rot (Table 2.1). The former develops from infections during blossom time, and the infection becomes clearly visible at the blossom end of the fruit by harvest time (Xu and Robinson 2010). Lenticel rot (Figure 2.3E) occurs during storage after a latency interval of several weeks as a result of infections originating from the field (Xu and Robinson 2010). During further storage, pale brown sporodochia of N. galligena are formed; these produce the highly diagnostic, elongated, 1- to 5-septate macroconidia of the Cylindrocarpon anamorph (Figure 2.3F). Lenticel rot caused by N. galligena has not so far been reported to be controlled by HWD. In fact, Maxin et al. (2005) found that its incidence increased after 1 min HWD at 49, 51 and 53°C compared to an untreated control, whereas there was no positive or negative influence on decay by 2 and 3 min HWD treatments. 2.3.3 Rubbery rot caused by Phacidiopycnis washingtonensis
Phacidiopycnis washingtonensis has only recently been identified as the cause of a fruit rot in American (Kim and Xiao 2006) and European (Weber 2011) apple production. From 2003–2006, in approximately 25% of the surveyed orchards of Washington State (USA), 1-4% of the apples were infected with P. washingtonensis (Kim and Xiao 2006). Following 9 months’ storage up to 24% losses caused by P.
washingtonensis were observed in ‘Red Delicious’ apples. Depending on the apple variety, invasion of P. washingtonensis occurred through stem end, calyx end, 12
Chapter 2: Literature review
lenticels or wounds (Kim and Xiao 2006; Weber 2012). The first report of P.
washingtonensis on apples in Europe was from the Lower Elbe region in Northern Germany, where fruit losses were below 1% in most orchards (Weber 2011). Mummified fruits of ‘Golden Hornet’ crabapples commonly planted as pollinators were identified as a major source of inoculum; fruit mummies of dessert apple varieties such as ‘Elstar’ were also infected, albeit to a lesser degree (Weber 2011). In Europe, cankers caused by P. washingtonensis have not yet been found. Mycelium of
P. washingtonensis may spread from an infected fruit to an adjacent intact fruit, causing clusters of rubbery rot (Weber 2012). Rubbery rot is a highly variable disease, appearing as a very pale but firm rot when fruit are removed from long-term storage under an atmosphere of reduced oxygen content, but rapidly undergoing a browning if sufficient oxygen becomes available during subsequent cold storage or at room temperature (Weber 2012). Conidiomata (pycnidia) are produced only on blackened fruit (Figure 2.3G). These extrude pale grey or yellow tendrils or drops of conidia which are hyaline, ellipsoid with pointed ends in outline, and contain two large or several smaller lipid droplets (Figure 2.3H). To date there are no reports on the efficacy of HWD on rubbery rot. 2.3.4 Bitter rot (anthracnose) caused by Colletotrichum acutatum
Colletotrichum acutatum has a wide range of hosts; both trees and fruit are infected by this pathogen. In Northern Europe, high pre- and postharvest fruit losses in strawberries, blueberries and cherries were attributed to C. acutatum (Sundelin et al. 2005; Børve and Stensvand 2006; Stensvand et al. 2006). C. acutatum has been reported as the most prevalent storage pathogen in Norway (Weber 2009b; Børve et al. 2010). In the rest of NW Europe, the relative importance of this fungus in stored apples is low, although losses may be on the increase (Weber 2009a). In subtropical and tropical areas, C. acutatum as well as C. gloeosporioides are well known pathogens (Peres et al. 2005). In apple orchards, conidia are splash-dispersed from buds formed during the previous growing season, and these may infect young leaves and fruit (Børve and Stensvand 2007). Fruit mummies and twig cankers cause infections on the maturing apples (Stensvand and Ren 2010). During storage, the development of C. acutatum decay is similar to Neofabraea spp. in that mycelium appears to grow from fungal spores deposited in the lenticels, colonizing the apple 13
Chapter 2: Literature review
within some weeks. The resulting lesion appears sunken and is often covered by dark grey mycelium extruding yellowish-pink spore drops (Figure 2.3I). Conidia are readily distinguished from N. perennans and N. alba in being straight, symmetrical and somewhat pointed at one or both ends (Figure 2.3J). However, a reliable distinction between C. acutatum and C. gloeosporioides is only possible by PCR analysis. Therefore it is important to determine by PCR if reports of infections of Swedish apples with G. cingulata (Tahir et al. 2009), teleomorph of C. gloeosporioides, can be confirmed. 2.3.5 Brown rot caused by Monilinia fructigena Brown rot caused by Monilinia fructigena is an important disease in apple orchards in Europe (Jijakli and Lepoivre 2004). High fruit losses due to M. fructigena have been reported in Hungary (Holb 2008), where up to 40% of apples were infected during the production phase in organically managed orchards. In comparison, orchards under IP management suffered losses up to 10% (Holb 2008). In the humid climate of NW Europe, the importance of M. fructigena is lower, 5% fruit loss from this fungus being regarded as high (Palm and Kruse 2005).
M. fructigena is a wound pathogen on apple fruit (Xu and Robinson 2000). Preharvest infections commonly occur in fruit that have been attacked by biting insects such as larvae of codling moth (Cydia pomonella) and leaf rollers (e.g. Adoxophyes orana). Mechanical damage caused by wind, birds, hailstorms or passing machinery in the alley ways may also result in M. fructigena infections (Holb 2008). The ability of M.
fructigena to infect a wound depends on the developmental stage of the fruit, wound age and the presence of free water or relative humidity above 97%. The highest rates of infection from M. fructigena have been observed in freshly (52°C). Hypothesis 8: The reduction of Penicillium rot in artificially inoculated apples is due to an effect of HWD on the fruit, not on the fungus. This hypothesis was accepted in Chapter 5, thereby also addressing hypotheses 5 and 6. In Section 8.3 general aspects on the acceptance of this hypothesis are discussed.
8.2 Effects of delayed ripening on the incidence of storage rots Apple storage methods have been revolutionized by the concepts of controlled atmosphere (CA) and dynamically controlled atmosphere (DCA) which enable fruit to be kept for much longer time periods than in cold storage under ambient atmosphere (Veltman et al. 2003). The main mode of action of CA and DCA is to delay fruit ripening. Treatment with 1-methyl-cyclopropene (1-MCP) achieves the same result through the different means of inhibiting ethylene production and 128
Chapter 8: General discussion
activity. However, none of these methods directly eliminates fungal inoculum. This explains why there are few, if any, synergies between 1-MCP and CA or DCA (Chapter 5). In terms of efficacy against the development of fungal postharvest diseases, CA or DCA after 8 months may be comparable to cold storage with 1-MCP after 6 months, or simple cold storage after 3 months (Spotts et al. 2007; Lafer 2010; see Chapter 6). In order to reduce the incidence of fruit rots after the end of a CA or DCA storage period, i.e. the time of fruit distribution, sale and consumption, fungal inoculum must be eliminated. This may be achieved by preharvest fungicide applications which are under public scrutiny, hygiene measures (e.g. removal of fruit mummies) which are labour-intensive and therefore costly, and HWD or HWR which have not (yet) gained full acceptance by fruit producers. The research presented in this Thesis indicates that these HWT hold significant unrealized potential. 8.2.1 Interactions between HWT and ripening inhibition A summary of existing literature knowledge of the efficacies of the above-mentioned methods to control postharvest diseases (pre-harvest fungicides, removal of mummies, low-temperature storage with or without CA or DCA, application of 1MCP) is presented in Table 8.1. The incidence of the major storage rots, caused by
Neofabraea spp., has been reported to be decreased by a delay in fruit ripening associated with CA, DCA, reduced storage temperatures, and 1-MCP (Spotts et al. 2007; Lafer 2010). The effect of CA on controlling blue mould caused by Penicillium
expansum may be due in part to a retarded fruit ripening, and partly to direct effects of the modified atmosphere on the fungus (Yackel et al. 1971). In contrast, other fungal storage rots such as Botrytis cinerea or Neonectria galligena were not affected by CA or DCA (Berrie et al. 2011). Similarly, the recently discovered Phacidiopycnis
washingtonensis failed to show any obvious response to CA, DCA and 1-MCP (Chapter 6). This provides a plausible explanation for the frequent discoveries of rubbery rot after prolonged DCA and CA storage (Weber 2011), in contrast to a lowered incidence of Neofabraea spp. under these conditions. Although, the efficacy of HWD against Neofabraea spp., P. expansum and M.
fructigena has been well documented (Burchill 1964; Maxin et al. 2005; Amiri and Bompeix 2010), recent reports have so far indicated a similar potential for HWR only 129
Chapter 8: General discussion
against P. expansum (Fallik et al. 2001). Prior to the publications originating from this Thesis, no literature existed on the efficacy of HWR on any other storage-rot fungus on apples. This Thesis has provided a new insight in to the potential of HWR and HWD in controlling major storage rot fungi (Table 8.1). In the present study high efficacies of both HWD and HWR were characterized for a wide range of storage-rot fungi including C. acutatum, Cladosporium spp., N galligena, P. washingtonensis, N. alba and N. perennans (Chapter 7). Further, P. expansum and B. cinerea were controlled in artificially infected fruit subjected to HWD (Chapter 5). These findings greatly expand our understanding of the potential offered by the physical HWT of apples. It is apparent from Table 8.1 that the range of fungi susceptible to HWD or HWR is wider than that of species controlled by 1-MCP, CA or DCA. Further, HWD and HWR can be expected to show synergies with ripening delay caused by CA, DCA or 1-MCP treatments because they are based on different modes of action. 8.2.2 Preharvest chemical treatments vs. postharvest HWT Efficacies of HWT in reducing storage rots and their possible positive interactions with any ripening delay procedures are an important basis for evaluating risks and benefits of HWR and HWD in the context of registration of new chemical substances in the EU for the use in plant protection (Section 2.6). The EU 2009/128/EC directive, which is currently being transformed into national legislation by all EU member states, requires that the new pesticide registration system “also establishes a mechanism for the substitution of more toxic pesticides by safer (including non-chemical) alternatives” (GD Health and Consumer, 2010). In providing such an alternative to chemical treatments, HWR and HWD may be expected to gain importance and acceptance as methods to control postharvest fungi in future. A similar focus may also be anticipated for preharvest hygiene measures aimed at reducing inoculum during the growing season or at harvest. These may consist of the removal of fruit mummies or sporulating cankers. However, although such measures may significantly reduce post-harvest decay caused by specific fungi (Holb and Scherm 2007), the efficacy of such measures against a wider range of species under NW European conditions remains to be proven. On biological grounds, synergistic effects between (1) hygiene measures, (2) HWT and (3) ripening delay caused by CA, DCA or 1-MCP may be expected.
130
Chapter 8: General discussion
8.3 The influence of heat on spores and fruit ‘Elstar’ apples artificially inoculated with Penicillium expansum and subjected to 3 min HWD at 55°C or above showed a higher incidence of blue mold than fruit subjected to HWD at 52°C. The choice of a relatively high temperature was based on the assumption that HWD Table 8.1: Efficacies of various methods for the reduction of post-harvest storage rots of apples, indicated as +++ (>75%), ++ (50-75%), + (50% and therefore provide a valuable tool that broadens options available to fruit growers and pack-house managers. Hot water treatments may be incorporated either pre- or post-storage into CA and DCA strategies and have the potential to reduce fruit wastage during the distribution and consumer phases and to enhance consumer satisfaction. The technology evaluated in this study showed that HWR gave rise to only slightly reduced disease control efficacies as compared to HWD, but that HWR holds several other advantages over HWD. The cost of HWR per unit of treated apples is expected to be much lower than for HWD because no additional labour is required and the amount of energy required to heat the water for a 30 s rinse should be about 20% of the energy used in a 3 min HWD process. A further advantage of HWR is that it can be incorporated into existing fruit grading lines, thus avoiding the need for additional equipment or parallel structures. Traditionally, harvested fruit in storage boxes are emptied by submersion in cold water, followed by floating the fruit to a conveyor belt, where they are dried and passed to the grading unit. Apples are then separated by size and pigmentation. Several exits on the grading unit are opened or closed, depending on the desired parameters. A HWR unit could easily be placed on such an exit, permitting a fraction of the total crop to be treated with hot water. Alternatively, all fruit could be treated by HWR prior to entering the drying unit. A closed HWR unit needs to be developed to minimize the emission of water vapor in the packing hall. Additional positive effects of HWR on fruit quality can be expected. In particular, it has been observed that fruit were less waxy and more homogenous following HWR and storage than after HWD or without hot-water treatments (see Section 4.2.3). Further, HWR may be associated with enhanced fruit firmness (Fallik et al. 2001). These attributes, which may be due to a partial melting of epicuticular waxes above 55°C (Aggarwal 2001), should be explored in future studies and may further address
135
Chapter 8: General discussion
Hypothesis 1 which war rejected based on the grounds of the preliminary work reported in this Thesis. Further research should also be aimed at identifying the proteins and/or lowmolecular weight substances induced by heat shock in apples. An understanding of their identity should enable us to optimise parameters and time-points of HWT in apples. An additional area of interest is a detailed characterisation of the responsiveness of fruit to HWR directly after harvest in comparison with fruit subjected to HWR after short- or long-term storage. Finally, the question remains whether apples treated by HWR before storage are capable of mounting an additional heatshock response if they are exposed to a second HWT during the packing phase, following a pre-storage HWR and, if so, how this might further improve fruit quality during the distribution phase.
.
136
Chapter 9: Literature Abbott WS (1925) A method for computing the effectiveness of an insecticide.
Journal of Economic Entomology 18, 265-267. Aggarwal P (2001) Phase transition of apple cuticles: a DSC study. Thermochimica
Acta 367, 9-13. Anderson PK, Cunningham AA, Patel PR, Morales FJ, Epstein PR, Daszak P (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends in Ecology and Evolution 19, 535-544. Amiri A, Bompeix G (2005a) Diversity and population dynamics of Penicillium spp. on apples in pre and postharvest environments: consequences for decay development.
Plant Pathology 54, 74-81. Amiri A, Bompeix G (2005b) Factors affecting the development of blue mould decay on apples. Phytoma 579, 27-31. Amiri A, Bompeix G (2005c) Micro-wound detection on apple and pear fruit surfaces using sulphur dioxide. Postharvest Biology and Technology 36, 51-59. Amiri A, Bompeix G (2010) Control of Penicillium expansum with potassium phosphite and heat treatment. Crop Protection 30, 222-227. Amiri A. and G. Bompeix 2011: Control of Penicillium expansum with potassium phosphite and heat treatment. Crop Protectio 30, 222–227. Amiri A, Dugas R, Pichot AL, Bompeix G (2009) In vitro and in vitro activity of eugenol oil (Eugenia caryophylata) against four important postharvest apple pathogens.
International Journal of Food Microbiology 129, 325-325. Batzer JC, Gleason ML, Weldon B, Dixon PM, Nutter FW (2002) Evaluation of postharvest removal of Sooty Blotch and Flyspeck on apples using sodium hypochlorite, hydrogen peroxide with peroxyacetic acid, and soap. Plant Disease 86, 1325-1332.
137
Chapter 9: Literature
Batzer JC, Hernández Rincon S, Mueller DS, Petersen BJ, Le Corronc F, McManus PS, Dixon PM, and Gleason ML (2010) Effect of temperature and nutrient concentration on the growth of six species of sooty blotch and flyspeck fungi. Phytopathologia
Mediterranea 49 3-10. Ben-Yehoshua S, Barak S, Shapiro B (1987) Postharvest curing at high temperature reduces decay of individual sealed lemons, pomelos, and other citrus fruits. Journal of
the American Society for Horticultural Science 112, 658–663. Beresford RM, Kim KS (2011) Identification of regional climatic conditions favorable for development of European canker of apple. Phytopathology 101, 135-146. Berrie AM (2007) Using rot risk assessment to minimise losses due to rots in cold stored apples. Novel approaches for the control of postharvest diseases and disorders. COST
Action 924 Proceedings of the International Congress: Novel approaches for the Control of Postharvest Diseases and Disorders Bologna, Italy, 443-447. Berrie AM, Xu X-M, Johnson D (2011) Lower temperatures more effective than atmosphere modification in controlling Botrytis and Nectria rots in stored apples.
Journal of Phytopathology 159, 73-79. Blanke MM, Burdick B (2005) Food (miles) for thought - Energy balance for locallygrown versus imported apple fruit. Environmental Science and Pollution Research 12, 125-127. Bollen GJ (1971) Resistance to Benomyl and some chemically related compounds in strains of Penicillium species. Netherlands Journal of Plant Pathology 77, 187-193. Bollen GJ, Scholten G (1971) Acquired resistance to Benomyl and some other systemic fungicides in a strain of Botrytis cinerea in cyclamen. Netherlands Journal of
Plant Pathology 77, 83-90. Bompeix G, Coureau C (2007) Practical use of thermotherapy against apple parasitic disorders. COST Action 924 Proceedings of the International Congress: Novel
138
Chapter 9: Literature
approaches for the Control of Postharvest Diseases and Disorders, Bologna, Italy, 149155. Børve J, Stensvand A (2006) Colletotrichum acutatum overwinters on sweet cherry buds. Plant Disease 90, 1452-1456. Børve J, Ren D, Stensvand A (2010) Alternative means to reduce storage decay in organic apple production; time of harvest and calcium applications. IOBC/WPRS
Bulletin 54, 61-64. Børve J, Stensvand A (2007) Colletotrichum acutatum found on apple buds in Norway. Plant Health Progress doi:10.1094/PHP-2007-0522-01-RS. Burchill R (1964) Hot water as a possible post harvest control of Gloeosporium rots of stored apples. Plant Pathology 13, 106-107. Bourke A (1991) Potato blight in Europe in 1845: the scientific controversy. In:
Pytophtora (Lucas JA, Shattock RC, Shaw DS, Cooke LR, eds.), 12-24. Cambridge: Cambridge University Press. Byers RE, Carbaugh DH, Combs LD (2004) Root restriction, an alternative to rootstocks, for control of flowering, fruiting, tree growth, yield efficiency, and fruit quality of apple.
Journal of Tree Fruit Production 3 (2), 11-31. Calabria G, Máca J, Bächli G, Serra L, Pascual M (2011) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. Journal of Applied
Entomology 136, 139-147 Casals C, Teixidó N, Viñas I, Silvera, E, Lamarca, N, Usall, J (2010) Combination of hot water, Bacillus subtilis CPA-8 and sodium bicarbonate treatments to control postharvest brown rot on peaches and nectarines. European Journal of Plant
Pathology 128, 51-63. Chmielewski FM, Muller A, Bruns E (2004) Climate changes and trends in phenology of fruit trees and field crops in Germany, 1961-2000. Agricultural and Forest
Meteorology 121, 69-78.
139
Chapter 9: Literature
Conway WS, Leverentz B, Janisiewicz WJ, Blodgett AB, Saftner RA, Camp MJ (2004) Integrating heat treatment, biocontrol and sodium bicarbonate to reduce postharvest decay of apple caused by Colletotrichum acutatum and Penicillium expansum.
Postharvest Biology and Technology 34, 11-20. Cunnington JH (2004) Three Neofabraea species on pome fruit in Australia.
Australasian Plant Pathology 33, 453-454. Delele MA, Vorstermans B, Creemers P, Tsige AA, Tijskens E, Schenk A, Opara UL, Nicolai BM, Verboven P (2012) CFD model development and validation of a thermonebulisation fungicide fogging system for postharvest storage of fruit. Journal
of Food Engineering 108, 59-68. DeLong JM, Prange RK, Harrison PA (1999) Using the Streif Index as a final harvest window for controlled-atmosphere storage of apples. HortScience 34, 1251-1255. EFSA (2010) Special Eurobarometer 354. European Food Safety Authority, doi:10.2805/51162. Einhorn ES, Logue J (2010) Can welfare states be sustained in a global economy? Lessons from Scandinavia. Political Science Quarterly 125, 1-29. Fallik E (2004) Prestorage hot water treatments (immersion, rinsing and brushing).
Postharvest Biology and Technology 32, 125-134. Fallik E, Alkalai-Tuvia S, Perzelan Y (2007) Prestorage hot water rinsing and brushing technology to reduce decay development in fresh produce. COST Action 924
Proceedings of the International Congress: Novel approaches for the Control of Postharvest Diseases and Disorders, Bologna, Italy, 141-148. Fallik E, Tuvia-Alkalai S, Feng X, Lurie S (2001) Ripening characterisation and decay development of stored apples after a short pre-storage hot water rinsing and brushing. Innovative Food Science and Emerging Technologies 2, 127-132. Fallik E, Aharoni Y, Copel A, Rodov V, Tuvia-Alkali S, Horev B, Yekuteli O, Wiseblum A, Regev R (2000) Reduction of postharvest loses of Galia melon by a short hot-water rinse. Plant Pathology 49, 333-338. 140
Chapter 9: Literature
Fallik E, Grinberg S, Alkalai S, Yekutieli O, Wiseblum A, Regev R, Beres H, Bar-Lev E (1999) A unique rapid hot water treatment to improve storage quality of sweet pepper. Postharvest Biology and Technology 15, 25-32. Fallik E, Grinberg S, Gambourg M, Klein J, Lurie S (1996) Prestorage heat treatment reduces pathogenicity of Penicillium expansum in apple fruit. Plant Pathology 45, 9297. Fallik E, Klein J, Grinberg S, Lomaniec E, Lurie S, Lalazar E (1993) Effect of postharvest heat treatment of tomatoes on fruit ripening and decay caused by Botrytis cinerea.
Plant Disease 77,985-988. Frasnelli K, Casera C, de Jager A, Johnson D, Hohn E (1996) Influence of harvest date on fruit quality and storability in the varieties Braeburn and Gala. The postharvest
treatment of fruit and vegetables. Determination and prediction of optimum harvest date of apples and pears; Proceedings of a COST Action 94 meeting, Lofthus, Norway, 9-10 June 1994, 105-115. Gariepy TD, Rahe JE, Levesque CA, Spotts R, Sugar D, Henriquez JL (2003) Analysis of putative Neofabraea isolates from bull's eye rot on stored pears from the Pacific Northwest by conventional and molecular methods suggests that N. alba is endemic in western North America. Canadian Journal of Plant Pathology 25, 109. Gariepy TD, Rahe JE, Levesque CA, Spotts RA, Sugar DL, Henriquez JL (2005)
Neofabraea species associated with bull's eye rot and cankers of apple and pear in the Pacific Northwest. Canadian Journal of Plant Pathology 27, 118-124. GD Health and Cosumers (2009) Directorate-General for Health and Consumers, European
Commission
http://ec.europa.eu/dgs/health_consumer/index_en.htm
ISBN 978-92-79-11599-8 Gleason ML, Batzer JC, Sun G, Zhang R, Aria MMD, Sutton TB, Crous PW, Ivanovic M, McManus PS, Cooley DR, Mayr U, Weber RWS, Yoder KS, Del Ponte EM, Biggs AR, Oertel B (2011) A new view of Sooty Blotch and Flyspeck. Plant Disease 95, 368-383. Granado J, Thuerig B, Kieffer E, Petrini L, Fliessbach A, Tamm L, Weibel FP, Wyss GS (2008) Culturable fungi of stored 'Golden Delicious' apple fruits: A one-season 141
Chapter 9: Literature
comparison study of organic and integrated production systems in Switzerland.
Microbial Ecology 56, 720-732. Guo LY, Michailides TJ (1997) Survival of Mucor piriformis in soil of apple orchards in California. Phytopathology 87, 37. Hennecke C, Koepcke D, Dierend W (2008) Dynamische Absenkung des Sauerstoffgehaltes bei der Lagerung von Äpfeln. Erwerbs-Obstbau 50, 19-29. Henriquez JL (2005) First report of apple rot caused by Neofabraea alba in Chile.
Plant Disease 89, 1360. Henriquez JL, Sugar D, Spotts RA (2004) Etiology of bull's eye rot of pear caused by
Neofabraea spp. in Oregon, Washington, and California. Plant Disease 88, 11341138. Henriquez JL, Sugar D, Spotts RA (2006) Induction of cankers on pear tree branches by Neofabraea alba and N. perennans, and fungicide effects on conidial production on cankers. Plant Disease 90, 481-486. Holb IJ (2008) Monitoring conidial density of Monilinia fructigena in the air in relation to brown rot development in integrated and organic apple orchards. European
Journal of Plant Pathology 120, 397-408. Holb IJ, Scherm H (2007) Temporal dynamics of brown rot in different apple management systems and importance of dropped fruit for disease development.
Phytopathology 97, 1104-1111. Holb IJ, Balla B, Abonyi F, Fazekas M, Lakatos P, Gall JM (2011) Development and evaluation of a model for management of brown rot in organic apple orchards.
European Journal of Plant Pathology 129, 469-483. Huang D, Haack RA, Zhang R (2011) Does global warming increase establishment rates of invasive alien species? A centurial time series analysis. PLoS ONE 6: e24733. doi:10.1371/journal.pone.0024733
142
Chapter 9: Literature
Jaeger SR, Andani Z, Wakeling IN, MacFie HJH (1998) Consumer preferences for fresh and aged apples: a cross-cultural comparison. Food Quality and Preference 9, 355-366 Jijakli M, Lepoivre P (2004) State of the art and challenges of postharvest disease
management in apples. In Mukerji, K.G. (Ed.), Fruit and Vegetable Diseases Vol. 1, Kluwer, Dordrecht, 59-94. Jones AL, Aldwinckle HS, (1990) Compendium of Apple and Pear Diseases. American Phytopathological Society, St. Paul, USA. Kader AA (2002) Postharvest Technology of Horticultural Crops. Agriculture and Natural Resources, University of California p. 338 Karabulut OA, Cohen L, Wiess B, Daus A, Lurie S, Droby S (2002) Control of brown rot and blue mold of peach and nectarine by short hot water brushing and yeast antagonists. Postharvest Biology and Technology 24, 103-111. Kennel W (1988) Massives Auftreten des Gloeosporium-Pilzes Pezicula malicortis.
Obst und Garten 107, 489-491. Kim YK, Xiao CL (2006) A postharvest fruit rot in apple caused by Phacidiopycnis
washingtonensis. Plant Disease 90, 1376-1381. Kim YK, Xiao CL (2008) Distribution and incidence of Sphaeropsis rot in apple in Washington State. Plant Disease 92, 940-946. Knoche M, Schröder M, Hinz M (2000) Control of the development of mummified fruit of 'Elstar' apple. Journal of Horticultural Science and Biotechnology 75, 328-335. Köhler W, Schachtel G, Voleske P (2007) Biostatistik: Einführung in die Biometrie für
Biologen und Agrarwissenschaftler. Springer-Verlag, Berlin, Heidelberg. Koreleska E, Etkowska A (2010) Market of organic food in Germany. Journal of
Research and Applications in Agricultural Engineering 55, 187-190. Kwon J-H, Kim J, Kim W-I (2011) First report of Rhizopus oryzae as a postharvest pathogen of apple in Korea. Mycobiology 39, 140-142. 143
Chapter 9: Literature
Lafer G (2010) Storability and fruit quality of organically grown 'Topaz' apples as affected by harvest date and different storage conditions. Acta Horticulturae 877, 795-798. Large EC (1940) The Advance of the Fungi. London: Jonathan Cape Leibinger W, Breuker B, Hahn M, Mendgen K (1997) Control of postharvest pathogens and colonization of the apple surface by antagonistic microorganisms in the field.
Phytopathology 87, 1103-1110. Lunn JA (1977) Rhizopus stolonifer. CMI Descriptions of Fungi and Bacteria 524. Lurie S (1998) Postharvest heat treatments. Postharvest Biology and Technology 14, 257-269. Lurie S, Klein JD (1990) Heat treatment of ripening apples: differential effects on physiology and biochemistry. Physiology of Plants 78, 181-186. Maguire KM, Lang A, Banks NH, Hall A, Hopcroft D, Bennett R (1999) Relationship between water vapour permeance of apples and micro-cracking of the cuticle.
Postharvest Biology and Technology 17, 89-96. Mari M, Torres R, Casalini L, Lamarca N, Mandrin JF, Lichou J, Larena I, De Cal MA, Melgarejo P, Usall J (2007) Control of post‐harvest brown rot on nectarine by
Epicoccum nigrum and physico‐chemical treatments. Journal of the Science of Food and Agriculture 87, 1271-1277. Maxin P, Fieger-Metag N, Benduhn B, Kruse P, Heyne P (2006) Hot water dipping in Northern German – on farm results after four years of scientific work. In: Proceedings
of the 12th International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing (Boos M, ed.). FÖKO, Weinsberg, Germany, 118120. Maxin P, Klopp K (2004) Economics of hot water dipping. In: Proceedings of the 11th
International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing (Boos M, ed.). FÖKO, Weinsberg, Germany, 75-78.
144
Chapter 9: Literature
Maxin P, Klopp K, Huyskens-Keil S, Ebert G (2005) Control of postharvest decay in organic grown apples by hot water treatment. Acta Horticulturae 682, 2153–2158. McCollum TG, D'Aquino S, McDonald RE (1993) Heat treatment inhibits mango chilling injury. HortScience 28, 197-198. McCracken AR, Berrie A, Barbara DJ, Locke T, Cooke LR, Phelps K, Swinburne TR, Brown AE, Ellerker B, Langrell SRH (2003) Relative significance of nursery infections and orchard inoculum in the development and spread of apple canker ( Nectria
galligena) in young orchards. Plant Pathology 52, 553-566. Minar P (2006) Effect of late summer treatments by strobilurines on storage diseases of apples. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 54(4), 39-43. Morales H, Marin S, Ramos AJ, Sanchis V (2010) Influence of postharvest technologies applied during cold storage of apples on Penicillium expansum growth and patulin accumulation: a review. Food Control 21, 953-962. Nega E, Ulrich R, Werner S, Jahn M (2003) Hot water treatment of vegetable seed – an alternative seed treatment method to control seed-borne pathogens in organic farming. Journal of Plant Diseases and Protection 110, 220-234. Neven LG, Mitcham EJ (1996) CATTS (controlled atmosphere/temperature treatment system): A novel tool for the development of quarantine treatments. American
Entomologist 42(1), 56-63. Nielsen, S. (2011) Håndbog for Frugt- og Baeravlere 2011. GartneriRådgivningen, Odense, Denmark. Palm G (2009) Pflanzenschutzmittel-Rückstände im Kernobst. Obst- und Weinbau 145(21), 8-11. Palm G (1997) Entwicklung der Bitterfäule während der CA/ULO- und Kühllagerung an Äpfeln. Mitteilungen des Obstbauversuchsringes des Alten Landes 52, 247-251.
145
Chapter 9: Literature
Palm G, Kruse P (2005) Maßnahmen zur Verminderung der Verluste durch Fruchtfäunis bei Apfel. Mitteilungen des Obstbauversuchsringes des Alten Landes 60, 46-52. Palm G, Kruse P (2007) Verhinderung von Lagerfäulen und Lagerschorf bei Äpfeln mit Heißwasser, Hefen, 1-MCP, Calcium-Salzen und Fungiziden. Mitteilungen des
Obstbauversuchsringes des Alten Landes 62, 231-236. Pavoncello D, Lurie S, Droby S, Porat R (2001) A hot water treatment induces resistance to Penicillium digitatum and promotes the accumulation of heat shock and pathogenesis-related proteins in grapefruit flavedo. Physiologia Plantarum 111, 1722. Pedersen DE (2006) Nettoprisen till avlere skal være mindst tre kroner. Frugt og Grønt 5, 218-219. Peres NA, Timmer LW, Adaskaveg JE, Correll JC (2005) Lifestyles of Colletotrichum
acutatum. Plant Disease 89, 784-796. Pierson CF (1966) Effect temperature on the growth of Rhizopus stolonifer on peaches and agar. Phytopathology 56, 276-278 Poldervaart G (2002) No more problems with skin spots of Elstar. Fruitteelt 92(13), 8-9. Poulsen ME, Naef A, Gasser S, Christen D, Rasmussen PH (2009) Influence of different disease control pesticide strategies on multiple pesticide residue levels in apple.
Journal of Horticultural Science and Biotechnology 84 (Special Issue), 58-61. Quast G, Weber RWS (2008) Aktuelles zu Infektionsbiologie von Diplodia seriata an Äpfeln im Niederelbegebiet. Mitteilungen des Obstbauversuchsringes des Alten
Landes 63, 373-380. R! Project, The R Project www.r-project.org Rappel, LM, Cooke AW, Jacobi KK, Wells IA (1991) Heat treatment for postharvest disease control in mangoes. Acta Hort. 291,362–371.
146
Chapter 9: Literature
Rizzoli W, Acler A (2009) Versuche zur Bekämpfung der Gloeosporium Fruchtfäule bei Pinova. Obst- und Weinbau 46, 267-271. Roelofs F (1996) Skin speckles occurring again. Fruitteelt 86(7), 11-12. Ranganna B, Raghavan GSV, Kushalappa AC (1998) Hotwater dipping to enhance storability of potatoes. Postharvest Biology and Technology 13, 215-223. Saure M (2007) Grundlagen der Reaktion von Apfelbäumen auf Wurzelschnitt – eine Übersicht. Erwerbs-Obstbau 49, 37-43. Sharp JL, Spalding DHJ (1984) Hot water as a quarantine treatment for Florida mangos infested with Caribbean fruit fly. Proceedings of the Florida State Horticultural
Society 97, 355-357. Schirmer H, Gräf V, Trierweiler B, Holland E (2004) Heißwasserbehandlung zur Reduzierung der Gloeosporium-Fäule. Obstbau 29, 440-443. Schirra M, D’Hallewin G, Ben-Yehoshua S, Fallik E (2000) Host-pathogen interactions modulated by heat treatment. Postharvest Biology and Technolgy 21, 71-85. Schulte, E (1997) Bitterfäule des Apfels – Infektion, Infektionsbedingungen, Auftreten im Lager, Bekämpfung. Ph.D. Thesis, University of Hanover, Germany. Schwartau H, Görgens M (2011) EU Kernobstschätzung 2011. Mitteilungen des
Obstbauversuchsringes des Alten Landes 66, 288-293. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (2007) Intergovernmental panel on climate change: synthesis report. Contribution of working group I, II and III to the fourth assessment report of the intergovernmental panel
on
climate
change.
http://www.ipcc.ch/pdf/assessment-
report/ar4/syr/ar4_syr.pdf Somia C, Palm G (1997) Einfluss unterschiedlich langer Einlagerungsphasen auf Fruchtfäulen beim Apfel im ULO Lager. Mitteilungen des Obstbauversuchsringes des
Alten Landes 52, 252-258.
147
Chapter 9: Literature
Sørensen JL, Phipps RK, Nielsen KF, Schroers H-J, Frank J, Thrane U (2009) Analysis of
Fusarium avenaceum metabolites produced during wet apple core rot. Journal of Agricultural and Food Chemistry 57, 1632-1639. Spadaro D, Garibaldi A, Gullino ML (2004) Control of Penicillium expansum and
Botrytis cinerea on apple combining a biocontrol agent with hot water dipping and acibenzolar-S-methyl, baking soda, or ethanol application. Postharvest Biology and
Technology 33, 141-151. Spotts RA, Chen PM (1987) Prestorage heat treatment for control of decay of pear fruit. Phytopathology 77, 1578–1582. Spolti P, Valdebenito-Sanhueza RM, Laranjeira FF, Del Ponte EM (2012) Comparative spatial analysis of the sooty blotch/flyspeck disease complex, bull’s eye and bitter rots of apples. Plant Pathololgy 61, 271-280. Spotts RA, Serdani M, Mielke EA, Bai J, Cehn PM, Hansen JD, Sanderson PG (2006) Effect of high-pressure hot water washing treatment on fruit quality, insects, and disease in apples and pears: Part II. Effect on postharvest decay of d’Anjou pear fruit.
Postharvest Biology and Technology 40, 216-220. Spotts RA, Sholberg PL, Randall P, Serdani M, Chen PM (2007) Effects of 1-MCP and hexanal on decay of d'Anjou pear fruit in long-term cold storage. Postharvest Biology
and Technology 44, 101-106. Spotts RA, Seifert KA, Wallis KM, Sugar D, Xiao CL, Serdani M, Henriquez JL (2009) Description of Cryptosporiopsis kienholzii and species profiles of Neofabraea in major pome fruit growing districts in the Pacific Northwest USA. Mycological Research 113, 1301-1311. Stensvand A, Ren D (2010) Sources of inoculum for Colletotrichum acutatum in cherry and apple. IOBC/WPRS Bulletin 54, 65-67. Stensvand A, Talgø V, Strømeng GM, Aamot HU, Børve J, Sletten A, Klemsdal S (2006)
Colletotrichum acutatum in Norwegian strawberry production and sources of potential inoculum in and around strawberry fields. Bulletin OILB/SROP 29(9), 87-91.
148
Chapter 9: Literature
Streif J (1983) Der optimale Erntetermin beim Apfel. I. Qualitätsentwicklung und Reife.
Gartenbauwissenschaft 48, 154-159. Streif J, Kittemann D, Neuwald DA, McCormick R, Xuan H (2010) Pre- and postharvest management of fruit quality, ripening and senescence. Acta Horticulturae 877, 55-68. Sundelin T, Schiller M, Lubeck M, Jensen DF, Paaske K (2005) First report of anthracnose fruit rot caused by Colletotrichum acutatum on strawberry in Denmark.
Plant Disease 89, 432. Sutton TB (1981) Production and dispersal of ascospores and conidia by
Physalospora
obtusa
and
Botryosphaeria
dothidae
in
apple
orchards.
Phytopathology 71, 584-589 Swinburne TR (1975) European canker of apple (Nectria galligena). Review of Plant
Pathology 54, 787-799. Tahir II, Johansson E, Olsson ME (2009) Improvement of apple quality and storability by a combination of heat treatment and controlled atmosphere storage. HortScience 44, 1648-1654. Thompson AK (2010) Controlled Atmosphere Storage of Fruits and Vegetables, second edition. CABI, Wallingford, UK. Trapman M (2004) A simulation program for the timing of fungicides to control Sooty Blotch in organic apple growing. In: Proceedings of the 11th International Conference
on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing (Boos M, Ed.). FÖKO, Weinsberg, Germany, 56-66. Trapman M, Jansonius PJ (2008) Disease management in organic apple orchards is more than applying the right product at the correct time. In: Proceedings of the 13th
International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing. FÖKO, Weinsberg, Germany, 16-22. Trapman M, Maxin P, Weber RWS (2008) Diplodia seriata, cause of black fruit rot in organically grown apples in Holland, Belgium and Northern Germany. In Proceedings
149
Chapter 9: Literature
of the 13th International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing. FÖKO, Weinsberg, Germany, 177-181. Trierweiler B, Schirmer H, Tauscher B (2003) Hot water treatment to control gloeosporium disease on apples during long-term storage. Journal of Applied Botany 77, 156-159. van Leeuwen GCM, van Kesteren HA (1998) Delineation of the three brown rot fungi of fruit crops (Monilinia spp.) on the basis of quantitative characteristics. Canadian
Journal of Botany 76, 2042-2050. Veltman RH, Verschoor JA, van Dugteren JHR (2003) Dynamic control system (DCS) for apples (Malus domestica Borkh. cv 'Elstar'): optimal quality through storage based on product response. Postharvest Biology and Technology 27, 79-86. Vorstermans B, Creemers P (2007) Screening preharvest/postharvest strategies to prevent fruit rot decay. Communications in Agricultural and Applied Biological
Sciences 72, 909-915. Vorstermans B, Creemers P, Bylemans D, Garnier A (2005) A new postharvest fungicide to control fruit rot on apple and pear. Communications in Agricultural and
Applied Biological Sciences 70, 79-89. Vorstermans B, Creemers P, Pujos P, Jijakli H, van Laer S (2007) Improving control of storage diseases on apple by combining biological and physical postharvest methods. Bulletin OILB/SROP 30(6/2), 423-426. Wang C (1994) Combined treatment of heat shock and low temperature conditioning reduces chilling injury in zucchini squash. Postharvest Biology and
Technology 4, 65-73 Wang CY, Bowen JH, Weir IE, Allan AC and Ferguson IB (2001) Heat-induced protection against death of suspension-cultured apple fruit cells exposed to low temperature. Plant Cell and Environment 24, 1199-1207. Warlop F, Bompeix G (2005) Relevance of hot water treatments for decay control.
Frutic 05, 134-140. 150
Chapter 9: Literature
Weber RWS (2009a) Betrachtung möglicher Auswirkungen des Klimawandels auf Schadpilze im Obstbau am Beispiel von Fruchtfäuleerregern an Äpfeln. Erwerbs-
Obstbau 51, 115-120. Weber RWS (2009b) Lagerfäulen an Äpfeln: Aktuelles aus Europa. Mitteilungen des
Obstbauversuchsringes des Alten Landes 64, 227-231. Weber RWS (2009c) Resistenz des Bitterfäule-Erregers Neofabraea perennans gegen Thiophanate-methyl: Konidienkeimung vs. Hyphenwachstum. Erwerbs-
Obstbau 51, 145-149. Weber RWS (2011) Phacidiopycnis washingtonensis, cause of a new storage rot of apples in Northern Europe. Journal of Phytopathology 159, 682-686. Weber RWS, Quast G (2009) Die Schwarze Sommerfäule des Apfels Obstbau 34, 388-390. Weber RWS, Palm G (2010) Resistance of storage rot fungi Neofabraea perennans,
N. alba, Glomerella acutata and Neonectria galligena against thiophanate-methyl in Northern German apple production. Journal of Plant Diseases and Protection 117, 185-191. Weber RWS (2012) Die Gummifäule, eine neue pilzliche Lagerfäule des Apfels in Europa. Mitteilungen des Obstbauversuchsringes des Alten Landes 67, 86-91. Weiss A, Mögel G, Kunz S (2006) Development of "Boni-Protect" - a yeast preparation for use in the control of postharvest diseases of apples. In: Proceedings of the 12th
International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing (Boos M, ed.). FÖKO, Weinsberg, Germany, 113-117. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols, a Guide to Methods and
Applications (Innis MA, Gelfand DJ, Sninsky JJ, White TJ, eds.). Academic Press, San Diego, USA, 315-322.
151
Chapter 9: Literature
Wilcke C (1996) Determination of harvest date of apple cultivars in Saxony. Cost 94
the Postharvest Treatment of Fruit and Vegetables - Determination and Prediction of Optimum Harvest Date of Apples and Pears, 67-75. Woolf AB, Ferguson I (2000) Postharvest responses to high fruit temperatures in the field. Postharvest Biology and Technology 21, 7-20. Woolf AB, Watkins CB, Bowen JH, Lay-Yee M, Maindonald JH, Ferguson IB (1995) Reducing external chilling injury in stored 'Hass' avocados with dry heat treatments.
Journal of the American Society for Horticultural Science 120, 1050-1056. Woolf AB, Ball S, Spooner KJ, Lay-Yee M, Ferguson IB, Watkins CB, Gunson A, Forbes SK (1997) Reduction of chilling injury in the sweet persimmon 'Fuyu' during storage by dry air heat treatments. Postharvest Biology and Technology 11, 155-164. Xu XM, Guerin L, Robinson JD (2001) Effects of temperature and relative humidity on conidial germination and viability, colonization and sporulation of Monilinia
fructigena. Plant Pathology 50, 561-568. Xu XM, Robinson JD (2000) Epidemiology of brown rot (Monilinia fructigena) on apple: infection of fruits by conidia. Plant Pathology 49, 201-206. Xu XM, Robinson JD (2010) Effects of fruit maturity and wetness on the infection of apple fruit by Neonectria galligena. Plant Pathology 59, 542-547. Yackel WC, Nelson AI, Wei LS, Steinberg MP (1971) Effect of controlled atmosphere on growth of mold on synthetic media and fruit. Applied and Environmental
Microbiology 22, 513-516. Yokoyama VY, Miller GT, Dowell RV (1991) Response of codling moth (Lepidoptera:
Tortricidae) to high temperature, a potential quarantine treatment for exported commodities. Journal of Economic Entomology 84, 528-531. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7, 203-214.
152
Chapter 9: Literature
Zhang H, Zheng X, Wang L, Li S, Liu R (2007) Effect of yeast antagonist in combination with hot water dips on postharvest Rhizopus rot of strawberries. Journal
of Food Engineering 78, 281-287. Zhang D, Lopez-Reyes JG, Spadaro D, Garibaldi A, Gullino ML (2010) Efficacy of yeast antagonists used individually or in combination with hot water dipping for control of postharvest brown rot of peaches. Journal of Plant Diseases and Protection 117, 226232. Zimmer J, Benduhn B, Mayr U, Kunz S, Rank H (2011) Erarbeitung einer Strategie zur Reduzierung des Kupfereinsatzes bei der Apfelschorfbekämpfung im ökologischen Obstbau. (organic eprints ID: 19277)
153