Eradication of plant pathogens and nematodes during composting: a review
The effects of temperature–time combinations and other sanitizing factors during composting on 64 plant pathogenic fungi, plasmodiophoromycetes, oomycetes, bacteria, viruses and nematodes were reviewed. In most cases pathogen survival was determined by bioassays of unknown sensitivity and minimum detection limits of 5% infection or more. For 33 out of 38 fungal and oomycete pathogens, all seven bacterial pathogens and nine nematodes, and three out of nine plant viruses, a peak temperature of 64–70°C and duration of 21 days, were sufficient to reduce numbers to below the detection limits of the tests used. Shorter periods and/or lower temperatures than those quoted in these tests may be satisfactory for eradication, but they were not always examined in detail in composting systems. Plasmodiophora brassicae (clubroot of Brassica spp.), Fusarium oxysporum f.sp. lycopersici (tomato wilt) and Macrophomina phaseolina (dry root rot) were more temperature-tolerant, as they survived a peak compost temperature of at least 62°C (maximum 74°C) and a composting duration of 21 days. Synchytrium endobioticum (potato wart disease) survived in water at 60°C for 2 h, but was not examined in compost. For Tobacco mosaic virus (TMV), peak compost temperatures in excess of 68°C and composting for longer than 20 days were needed to reduce numbers below detection limits. However, TMV and Tomato mosaic virus (TomMV) were inactivated over time in compost, even at temperatures below 50°C. Temperatures in excess of 60°C were achieved in different composting systems, with a wide range of organic feedstocks. The potential survival of plant pathogens in cooler zones of compost, particularly in systems where the compost is not turned, has not been quantified. This may be an important risk factor in composting plant wastes.
Concerns about the presence of plant pathogens and nematodes are a limitation to the increased uptake of composted organic waste by potential end-users in the horticultural and agricultural sectors. For convenience, in this review eradication is defined as a reduction in the levels of a pathogen to below the limit of detection of the specific detection method used. As no detection assay can give an absolute guarantee that compost is free from a particular pathogen, this means that in some cases low levels of the pathogen in question may still be present in the compost.
Bollen & Volker (1996) and Ryckeboer (2001) have previously reviewed survival and eradication of plant pathogens and nematodes during composting. The aim of this review is to collate the available data from these and other sources, together with estimated detection limits, so that recommendations for the phytosanitary requirements of composting could be made.
The composting process normally consists of three phases that can be more-or-less distinct: an initial mixing period with mesophilic growth; a high-temperature thermophilic phase (or sanitization); and a longer and lower temperature mesophilic phase (maturation or stabilization) (Day & Shaw, 2001). The success of composting in eliminating pathogens is not solely a result of the heating process, but also depends on the many and complex microbial interactions that may occur, as well as other compost parameters such as moisture content (Bollen, 1985). According to Bollen (1985), the eradication of pathogens from organic wastes during composting is primarily due to: (i) heat generated during the thermophilic phase of the composting process; (ii) the production of toxic compounds such as organic acids and ammonia; (iii) lytic activity of enzymes produced in the compost; and (iv) microbial antagonism, including the production of antibiotics and parasitism.
Other factors involved in eradication are: (v) competition for nutrients (Ryckeboer, 2001); (vi) natural loss of viability of the pathogen with time (Coventry et al., 2002); and (vii) compounds that stimulate the resting stages of pathogens into premature germination (Coventry et al., 2002).
However, heat generated during the thermophilic high-temperature phase of aerobic composting appears to be the most important factor for the elimination of plant pathogens (Bollen & Volker, 1996). Although pathogen numbers may continue to decline during compost maturation, the conditions are more difficult to define for sanitization standards, and are less likely to be conducive for reliable pathogen eradication than the high-temperature phase. The combinations of temperature and duration of exposure are referred to as temperature–time effects in this review.
Systems used for studying temperature–time effects on eradication
The pathogen and nematode species covered in this review, together with their hosts and the common names of the associated diseases, are listed in Table 1. These are mainly soilborne organisms as these are usually considered to pose the greatest risk in subsequent use of composted materials. Most of this research has been conducted during aerobic composting of organic wastes, although data on pathogen eradication in anaerobic digester liquid, soil, agar, water and plant material with dry heat or steam–air is also shown for comparison. For some organisms (e.g. Pythium ultimum), only data obtained in noncomposting systems are available. For tests conducted in compost a range of feedstocks have been used, although the most widely used materials were various crop or plant residues, including ‘green’ or ‘yard’ waste (a mixture of leaves, prunings and grass clippings from parks and gardens). Other feedstocks used in eradication tests were municipal organic wastes or ‘biowastes’ (Menke & Grossmann, 1971; Christensen et al., 2001), bark (Hoitink et al., 1976) or woodchips (Bruns et al., 1993). Some authors included nitrogenous materials or ‘activators’ such as animal manures (Lopez-Real & Foster, 1985; Dittmer et al., 1990) or inorganic nitrogen sources (Hoitink et al., 1976; Coventry et al., 2001).
Table 1. Plant pathogens and nematodes covered in this review, hosts and common name of diseases caused, or of nematodes
|Armillaria mellea||various woody||honey fungus|
|Botrytis aclada (syn. allii)||onion (Allium cepa)||neck rot|
|Botrytis cinerea||various||grey mould|
|Didymella lycopersici||tomato (Lycopersicon esculentum)||stem rot|
|Fusarium oxysporum f.sp. callistephi||Aster spp.||wilt|
|F. oxysporum f.sp. dianthi||carnation, pink (Dianthus spp.)||wilt|
|F. oxysporum f.sp. lilii||lily (Lilium spp.)||scale rot|
|F. oxysporum f.sp. lycopersici||tomato (L. esculentum)||wilt|
|F. oxysporum f.sp. melongenae||egg plant (Solanum melongena)||wilt|
|F. oxysporum f.sp. melonis||melon (Cucumis melo)||wilt|
|F. oxysporum f.sp. narcissi||Narcissus spp.||basal rot|
|F. oxysporum f.sp. pisi||pea (Pisum sativum)||wilt|
|Fusarium solani f.sp. cucurbitae||Cucurbitaceae||wilt|
|Macrophomina phaseolina||various||dry root rot|
|Olpidium brassicae||various||vectors of LBVV and TNV|
|Phomopsis sclerotioides||cucumber (Cucumis sativus)||black rot|
|Pseudocercosporella herpotrichoides||wheat (Triticum aestivum)||foot rot|
|Pyrenochaeta lycopersici||tomato (L. esculentum)||corky root|
|Rhizoctonia solani||various potato black-scurf||damping-off,|
|Sclerotinia fructigena||stone fruits (Prunus spp.)||brown rot|
|Sclerotinia sclerotiorum||various||watery soft rot|
|Sclerotium cepivorum||Allium spp.||white rot|
|Sclerotium (Corticium) rolfsii||various||southern blight|
|Septoria lycopersici||tomato (L. esculentum)||leaf spot|
|Stromatinia gladioli||Gladiolus spp.||dry rot|
|Synchytrium endobioticum||potato (Solanum tuberosum)||wart disease|
|Taphrina deformans||peach (Prunus persica)||leaf curl|
|Thielaviopsis basicola||various||black root rot|
|Verticillium albo-atrum||hop (Humulus lupulus)||wilt|
|Polymyxa betae||Chenopodiacae||vector of BNYV|
|Phytophthora cinnamomi||various||root rot, dieback|
|Phytophthora cryptogea||various||collar rot, root rot|
|Phytophthora infestans||potato (S. tuberosum)||potato blight|
|tomato (L. esculentum)|| |
|Phytophthora ramorum||various woody||sudden oak death|
|Pythium irregulare||various||root rot|
|Pythium ultimum||various||damping-off, root rot|
|Clavibacter michiganensis ssp. michiganensis||tomato (L. esculentum)||canker|
|Erwinia amylovora||Rosaceae||fire blight|
|Erwinia carotovora ssp. atroseptica||potato (S. tuberosum)||black leg and soft rot|
|Erwinia carotovora ssp. carotovora||various||soft rot|
|Erwinia chrysanthemi||various||soft rot, blight|
|Pseudomonas savastanoi pv. phaseolicola||Phaseolus beans|| |
|Ralstonia solanacearum||Solanaceae||bacterial wilt|
|Cucumber green mottle mosaic (CGMMV)||cucumber (Cucumis sativus)|| |
|Lettuce big vein (LBVV)||lettuce (Lactuca sativa)|| |
|Melon necrotic spot||Cucurbitaceae|| |
|Pepper mild mottle||Solanaceae|| |
|Tobacco mosaic (TMV)||various|| |
|Tobacco necrosis (TNV)||various|| |
|Tobacco rattle (TRV)||various|| |
|Tomato mosaic (ToMV)||various|| |
|Tomato spotted wilt virus||various|| |
|Aphelenchoides ritzemabosi||Chrysanthemum spp. strawberry (Fragaria spp.)|| |
|Globodera pallida||potato (S. tuberosum),||white potato cyst|
|tomato (L. esculentum)|| |
|Globodera rostochiensis||potato (S. tuberosum),||yellow potato cyst|
|tomato (L. esculentum)|| |
|Heterodera schachtii||beet (Beta vulgaris)||beet cyst|
|Meloidogyne hapla||potato (S. tuberosum)||northern root-knot|
|Meloidogyne incognita||beet (B. vulgaris)||southern root-knot|
|Meloidogyne javanica||various||Javanese root-knot|
|Pratylenchus penetrans||strawberry (Fragaria spp.),||meadow|
Where eradication tests were conducted in compost, these were mostly conducted in self-heating heaps (piles) of varying size, with or without forced aeration or turning. The temperatures within such heaps varied in both space and time. Bollen et al. (1989) and Bollen (1993) quote a maximum compost temperature for the heat phase of the tests. During this heat phase, compost temperatures increased from ambient to these maximum values and back down to ≈ 30 °C over a period of 3–4 weeks. The eradication and survival temperatures during composting in Tables 2–9 are the maximum or average values during the specified times, which were normally part or all of the heat phase of the composting test. The composting tests of Coventry et al. (2001) were conducted in thermostatically controlled aerated flasks at constant temperature. Where eradication data were obtained in other (noncomposting) test systems (Table 4), the test material was directly exposed to dry heating in an incubator or indirectly heated in a water bath or similar equipment. In these other test systems, the temperatures were generally determined more accurately than in composting systems. The reliability of the data will depend on the accuracy and calibration of the temperature-monitoring equipment, as well as the proximity of the test pathogen to the monitoring probe.
Table 2. Temperature–time conditions for eradication of plant pathogenic fungi, plasmodiophoromycetes and oomycetes in compost
|Armillaria mellea||cherry wood||garden refuse||70|| 21||plating||PDA||12% res||Yuen & Raabe (1984)|
|Botrytis aclada||bulbs/sclerotia||garden refuse||64–70|| 21||bioassay||onion bulbs||5% inf||Bollen et al. (1989)|
|Botrytis cinerea||bean leaves||grass, hop waste, manure||35|| 4||bioassay||bean||?||Lopez-Real & Foster (1985)|
|B. cinerea||geranium stems/leaves||bark||60|| 91||plating||selective agar||4% res||Hoitink et al. (1976)|
|Colletotrichum coccodes||tomato, aubergine roots/stems||garden refuse||64–70|| 21||bioassay||aubergine||5% inf||Bollen et al. (1989)|
|Didymella lycopersici||tomato haulms||inoculum||59–73|| 7||bioassay||tomato||8% inf||Phillips (1959)|
|f.sp. callistephi||Chinese aster||garden refuse||47–65|| 21||bioassay||Chinese aster||8% inf||Bollen et al. (1989)|
|f.sp. lilii||lily bulbs||garden refuse||58–70|| 21||bioassay||lily bulb scales||> 3% inf||Bollen et al. (1989)|
|f.sp. melonis||melon roots/stems||garden refuse||56–67|| 21||bioassay||melon||4% inf||Bollen et al. (1989)|
|f.sp. melonis||melon residue||plant residues||64|| 4||plating||PDA||?||Suarez-Estrella et al. (2003)|
|f.sp. narcissi||bulb peelings||plant residues||40||210||?||?||?||Bollen et al. (1991)|
|Fusarium solani f.sp. cucurbitae||courgette roots/stems||garden refuse||53–65|| 21||bioassay||courgette||8% inf||Bollen et al. (1989)|
|Phomopsis sclerotioides||gherkin roots||garden refuse||64–70|| 21||bioassay||gherkin||> 4% inf||Bollen et al. (1989)|
|Pseudocercosporella herpotricoides||mycelium||green waste, straw||60|| 7||plating||water agar + antibiotics||?||Dittmer et al. (1990)|
|Pyrenochaeta lycopersici||tomato roots||garden refuse||53–65|| 21||bioassay||tomato||5% inf||Bollen et al. (1989)|
|Rhizoctonia solani||potato tubers/sclerotia||garden refuse||64–70|| 21||bioassay||potato||> 13% inf||Bollen et al. (1989)|
|R. solani||millet seed||garden refuse, sawdust||70|| 21||plating||water agar||12% res||Yuen & Raabe (1984)|
|R. solani||beet pieces||bark||50|| 77||bioassay||beet||2% inf||Hoitink et al. (1976)|
|R. solani||wheat kernels||household, various||52 av|| 49||bioassay + ELISA||bean||> 9% inf ||Christensen et al. (2001)|
|Sclerotinia sclerotiorum||lettuce stems/sclerotia||garden refuse||64–70|| 21||bioassay||cucumber||> 5% inf||Bollen et al. (1989)|
|S. sclerotiorum||sclerotia||green waste, manure||74|| 23||fluorescence microscope||fluorescein diacetate||5% scler||Dittmer et al. (1990)|
|S. sclerotiorum||sclerotia||biowaste||74|| 18||plating||PDA||?||Hermann et al. (1994)|
|Sclerotium cepivorum||bulbs/sclerotia||garden refuse||64–70|| 21||bioassay||onion||> 8% inf||Bollen et al. (1989)|
|S. cepivorum||sclerotia||onion waste (flasks)||48 const|| 3||plating||PDA||2% scler||Coventry et al. (2002)|
|Sclerotium rolfsii||sclerotia||spice–sawdust||32|| 12||plating||water agar||2% scler||Yuen & Raabe (1984)|
|Stromatinia gladioli||gladiolus leaves/sclerotia||garden refuse||64–70||21||bioassay||gladiolus||2% inf||Bollen et al. (1989)|
|Thielaviopsis basicola||spores||?||63||?||heap||?||?||Grushevoi & Levykh (1940)|
|Verticillium dahliae||rose stems||garden refuse, sawdust||70||21||plating||cellophane agar||20% res||Yuen & Raabe (1984)|
|Plasmodiophora brassicae||cabbage roots||garden refuse||47–65||21||bioassay||Chinese cabbage||> 8% inf||Bollen et al. (1989)|
|P. brassicae||cabbage roots||grass, hop waste, manure||54 av|| 1||bioassay||cabbage||?||Lopez-Real & Foster (1985)|
|P. brassicae||galls/soil||household, woodchips||60–80||49||bioassay||cauliflower||9% inf||Bruns et al. (1993)|
|P. brassicae||galls/soil||household, various||49 av||14||bioassay||Brassica juncea||> 7% inf||Christensen et al. (2001)|
|P. brassicae||cauliflower roots/soil||biowaste or green waste||60 av|| 2||bioassay||Brassica juncea||?||Ryckeboer (2001)|
|Phytophthora cinnamomi||rhododendron crown/roots||bark||50||77||baiting + plating||lupin||?||Hoitink et al. (1976)|
|Phytophthora cryptogea||Chinese aster root clods||garden refuse||64–70||21||bioassay||Chinese aster||> 5% inf||Bollen et al. (1989)|
|Phytophthora infestans||potato tubers||garden refuse||47–65||21||bioassay||potato disks||3% inf||Bollen et al. (1989)|
|Phytophthora ramorum||oak wood, laurel leaves||wood chips, green waste||?||14||bioassay||pear||?||Garbelotto (2003)|
|Pythium irregulare||rhododendron crown/roots||bark||50||77||baiting + plating||lupin||?||Hoitink et al. (1976)|
Table 3. Temperature–time conditions for survival of plant pathogenic fungi and plasmodiophoromycetes in compost
|Didymella lycopersici||tomato haulms||inoculum||56|| 27||bioassay||tomato||Phillips (1959)|
|f.sp. lycopersici||wheat kernels||household, various||74|| 21||bioassay||tomato||Christensen et al. (2001)|
|f.sp. melongenae||aubergine root clods||garden refuse||53–65|| 21||bioassay||aubergine||Bollen et al. (1989)|
|f.sp. pisi||mycelium/soil||onion waste (flasks)||50 const|| 7||platingb||komada||Coventry et al. (2001)|
|Macrophomina phaseolina||infected roots||crop, weed residues||60–62|| 21||plating||selective agar||Lodha et al. (2002)|
|Olpidium brassicae||lettuce root clods||garden refuse||56–67|| 21||bioassayb||lettuce||Bollen et al. (1989)|
|Rhizoctonia solani||wheat kernels||household, various||57 av|| 14||bioassay + ELISA||bean||Christensen et al. (2001)|
|Sclerotinia sclerotiorum||sclerotia||green waste, straw||42|| 23||fluorescence microscope||fluorescein diacetate||Dittmer et al. (1990)|
|Plasmodiophora brassicae||naturally present||sludge, manure, feathers||70||175||bioassay||Brassica nigra||Ylimaki et al. (1983)|
|P. brassicae||galls, soil||household, woodchips||40–60|| 98||bioassay||cauliflower||Bruns et al. (1993)|
|P. brassicae||galls, soil||biowaste||60||182||bioassay||Brassica juncea||Ryckeboer et al. (2002b)|
Table 4. Temperature–time conditions for eradication of plant pathogenic fungi, plasmodiophoromycetes and oomycetes in other systems
|Armillaria mellea||citrus roots||inoculum||41||7 h||steam–air||direct plating||agar||18% inf||Munnecke et al. (1976)|
|A. mellea||infected plants||inoculum||49||30 min||steam–air||direct plating||agar||18% inf||Munnecke et al. (1976)|
|Botrytis cinerea||geranium stems/leaves||inoculum||40||21 days||incubator||direct plating||PDA, selective agar||5% res||Hoitink et al. (1976)|
|B. cinerea||geranium stems/leaves||inoculum||50||7 days||incubator||direct plating||PDA, selective agar||5% res||Hoitink et al. (1976)|
|B. cinerea||spores||water||47||4 min||water||direct plating||agar||0·25% res||Smith (1923)|
|B. cinerea||spores||water||50||6 min||water||direct plating||agar||0·25% res||Smith (1923)|
|B. cinerea||conidia||water||65||10 min||water||bioassay||bean||?||Lopez-Real & Foster (1985)|
|Fusarium oxysporum||suspension||sewage||35||3 days||anaerobic||enrichment||Czapek Dox and PSA||30 prop/mL||Turner et al. (1983)|
|f.sp. dianthi|| ||sludge|| || ||digester||plating|| || || |
|f.sp. melonis||melon residues||inoculum||55||4 days||incubator||plating||PDA||?||Suarez-Estrella et al. (2003)|
|Olpidium brassicae||sporangia||water||50||10 min||water bath||bioassay||lettuce||12·5% spora||Campbell & Lin (1976)|
|Rhizoctonia solani||barley seed||inoculum||40||49 days||incubator||direct plating||PDA and water agar||?||Hoitink et al. (1976)|
|R. solani||barley seed||inoculum||50||7 days||incubator||direct plating||PDA and water agar||?||Hoitink et al. (1976)|
|R. solani||mycelium||water||50||7 min||water||direct plating||PDA||?||Miller & Stoddard (1956)|
|R. solani||mycelium||agar||50||12 min||water bath||direct plating||PDA||2% res||Pullman et al. (1981)|
|Sclerotinia fructigena||infected plants||?||52||?||?||?||?||?||Spector (1956)|
|Sclerotinia minor||sclerotia||soil||50||1·5 days||incubator||direct plating||semiselective||6% scler||Adams (1987)|
|Sclerotinia sclerotiorum||sclerotia||inoculum||50||39 days||incubator||direct plating||PDA||?||Hermann et al. (1994)|
|S. sclerotiorum||sclerotia||inoculum||70||4 days||incubator||direct plating||PDA||?||Hermann et al. (1994)|
|S. sclerotiorum||sclerotia||soil||60||3 min||steam–air||direct plating||PDA, semiselective||3·5% scler||van Loenen et al. (2003)|
|S. cepivorum||sclerotia||soil||40||8 days||incubator||direct plating||PDA||1% scler||McLean et al. (2001)|
|S. cepivorum||sclerotia||soil||45||12 h||incubator||direct plating||PDA||1% scler||McLean et al. (2001)|
|S. cepivorum||sclerotia||soil||50||6 h||incubator||direct plating||PDA||1% scler||McLean et al. (2001)|
|S. cepivorum||sclerotia||soil||45||1·7 days||incubator||direct plating||semiselective||6% scler||Adams (1987)|
|S. cepivorum||sclerotia||soil||50||19 h||incubator||direct plating||semiselective||6% scler||Adams (1987)|
|S. cepivorum||sclerotia||soil||50||3 min||steam–air||direct plating||PDA||2·5% scler||van Loenen et al. (2003)|
|Septoria lycopersici||spores||?||43||?||water||?||?||?||Spector (1956)|
|Synchytrium endobioticum||sporangia||water||60||8 h||water bath||staining||acid fuchsin||7% spora||Glynne (1926)|
|Taphrina deformans||mycelium||?||46||?||?||?||?||?||Spector (1956)|
|Thielaviopsis basicola||mycelium||agar||45||15 h||water bath||direct plating||PDA||2% res||Pullman et al. (1981)|
|T. basicola||mycelium||agar||50||1·3 min||water bath||direct plating||PDA||2% res||Pullman et al. (1981)|
|Verticillium albo-atrum||hop vine||inoculum||50||3 h||water bath||direct plating||PLY agar||?||Talboys (1961)|
|V. albo-atrum||hop vine||inoculum||55|| 1 h||water bath||direct plating||PLY agar||?||Talboys (1961)|
|V. albo-atrum||hop vine||inoculum||60||15 min||water bath||direct plating||PLY agar||?||Talboys (1961)|
|V. albo-atrum||mycelium||water||53|| 4 min||water bath||direct plating||PDA||?||Miller & Stoddard (1956)|
|V. albo-atrum||microsclerotia||water||55|| 4 min||water bath||direct plating||PDA||?||Miller & Stoddard (1956)|
|V. albo-atrum||mycelium||plant stem||47|| 5 min||water||direct plating||barley straw agar||?||Nelson & Wilhelm (1958)|
|V. albo-atrum||microsclerotia||plant stem||47||40 min||water||direct plating||barley straw agar||?||Nelson & Wilhelm (1958)|
|Verticillium dahliae||mycelium||agar||45|| 8 h||water bath||direct plating||PDA||2% res||Pullman et al. (1981)|
|V. dahliae||mycelium||agar||47|| 2 h||water bath||direct plating||PDA||2% res||Pullman et al. (1981)|
|V. dahliae||microsclerotia||soil||50|| 3 min||steam–air||direct plating||selective agar||2·5% res||van Loenen et al. (2003)|
|Plasmodiophora brassicae||filtered extract||water||75||10 min||water||bioassay||cabbage||?||Lopez-Real & Foster (1985)|
|P. brassicae||roots/soil||biowaste||52||10 h||anaerobic digester||bioassay||Brassica juncea||25% inf||Ryckeboer et al. (2002a)|
|Phytophthora cinnamomi||rhododendron crown/roots||inoculum||40|| 7 days||incubator||direct plating||selective agar||?||Hoitink et al. (1976)|
|Phytophthora infestans||mycelium||water||45||?||water||?||?||?||Spector (1956)|
|P. infestans||spores||water||25||?||water||?||?||?||Spector (1956)|
|Phytophthora ramorum||wood chips/bay leaves||inoculum||55||14 days||incubator||direct plating||selective agar||?||Garbelotto (2003)|
|Pythium ultimum||infected Aloe plants||water||46||45 min||water||bioassay||Aloe variegata||?||Baker & Cummings (1943)|
|P. ultimum||mycelium||agar||45|| 9 h||water bath||direct plating||PDA||2% res||Pullman et al. (1981)|
|P. ultimum||mycelium||agar||50||33 min||water bath||direct plating||PDA||2% res||Pullman et al. (1981)|
|P. ultimum||mycelium||soil||50|| 3 min||steam–air||bioassay||pea||?||van Loenen et al. (2003)|
|Pythium irregulare||rhododendron crown/roots||inoculum||40|| 7 days||incubator||baiting + plating||lupin||?||Hoitink et al. (1976)|
Table 5. Temperature–time conditions for eradication of bacterial plant pathogens in compost and other systems
|Erwinia amylovora||cotoneaster shoots||biowaste, woodchips||> 40 max|| 7 days||heap||dilution plating||M–S||> 300 cfu g−1||Bruns et al. (1993)|
|E. amylovora||suspension||biowaste||55 max||56 h||aerated tunnel||dilution plating||selective||?||Ryckeboer (2001)|
|Erwinia chrysanthemi||chrysanthemum||bark||60 max||77 days||heap||dilution plating||selective||8% res||Hoitink et al. (1976)|
|Pseudomonas savastanoi pv. phaseolicola||bean leaves||grass, hop waste, manure||35 max|| 4 days||heap||bioassay||bean||?||Lopez-Real & Foster (1985)|
|Ralstonia solanacearum||potato pieces||biowaste||59 max||16 h||aerated tunnel||dilution plating||selective agar||20 cfu mL−1 digest 1E3 cfu g−1 infected material||Ryckeboer (2001)|
|In other systems|
|Clavibacter michiganensis ssp. michiganensis||suspension||sewage sludge, tomato||35 av|| 7 days||anaerobic digester||enrichment and dilution plating||D2 broth & nutrient agar||3E3 cfu mL−1||Turner et al. (1983|
|E. amylovora||suspension||inoculum||50 const||30 min||water bath||dilution plating||KB||?||Keck et al. (1995)|
|E. amylovora||apple budwood||inoculum||45c const|| 3 h||incubator||dilution plating||KB||9% inf||Keck et al. (1995)|
|Erwinia carotovora ssp. atroseptica||suspension||inoculum||50 const||15 min||water bath||dilution plating||nutrient agar||?||Robinson & Foster (1987)|
|Erwinia carotovora ssp. carotovora||suspension||inoculum||50 const||30 min||water bath||dilution plating||nutrient agar||?||Robinson & Foster (1987)|
|E. chrysanthemi||suspension||inoculum||50 const||40 min||water bath||dilution plating||nutrient agar||?||Robinson & Foster (1987)|
|E. chrysanthemi||chrysanthemum||inoculum||40 const|| 7 days||incubator||dilution plating||selective||10% res||Hoitink et al. (1976)|
|P. savastanoi pv. phaseolicola||filtered leaf macerate||inoculum||65 const||10 min||water bath||bioassay||bean||?||Lopez-Real & Foster (1985)|
|R. solanacearum||suspension||biowaste||52 const||12 h||anaerobic digester||dilution plating||selective agar||20 cfu mL−1 digest 1E3 cfu g−1 infected material||Ryckeboer et al. (2002a)|
Table 8. Temperature–time conditions for eradication of plant parasitic nematodes in compost and other systems
|Globodera rostochiensis||cysts||potatoes||33 const||?||heap||?||?||?||Sprau (1967)|
|Heterodera schachtii||cysts||biowaste||67 max||62 h||vessels||larval emergence||ZnCl2 soln||4% cyst||Ryckeboer (2001)|
|Meloidogyne chitwoodii||infected tubers of Scorzonera||biowaste||58 av||42 h||aerated tunnels||bioassay||tomato||?||Ryckeboer (2001)|
|Meloidogyne incognita||pepper/tomato||refuse||57 av||19 h||compost silo||bioassay||gherkin||9% inf||Menke & Grossmann (1971)|
|M. incognita||egg sacs||biowaste||74 max|| 4 days||heap||bioassay||pepper||9% inf||Hermann et al. (1994)|
|M. incognita||egg sacs||biowaste||50 const||30 h||incubator||bioassay||pepper||9% inf||Hermann et al. (1994)|
|In other systems|
|Aphelenchoides ritzemabosi||infected bulbs||inoculum||45 const|| 3 h||water bath||?||?||?||Becker (1974)|
|Globodera pallida||cysts||soil||50 const|| 3 min||steam–air||larval emergence||diffusate||7·5% cyst||van Loenen et al. (2003)|
|Globodera rostochiensis||cysts||soil||60 const|| 3 min||steam–air||larval emergence||diffusate||7·5% cyst||van Loenen et al. (2003)|
|Meloidogyne hapla||strawberry roots||inoculum||49 const|| 7 min||water bath||bioassay/microscopy||water||30% inf||Goheen & McGrew (1954)|
|M. hapla||rose roots||inoculum||45·5 const|| 1 h||water bath||larval emergence||rose||?||Martin (1968)|
|M. incognita||tomato roots||biowaste||52 const||12 h||anaerobic digester||bioassay||tomato||25% inf||Ryckeboer et al. (2002a)|
|Meloidogyne javanica||potato tubers||inoculum||46 const|| 2 h||water bath||bioassay||tomato||50% inf||Martin (1968)|
|M. javanica||potato tubers||inoculum||49 const|| 1 h||water bath||bioassay||tomato||50% inf||Martin (1968)|
|Pratylenchus penetrans||strawberry roots||inoculum||46 const||45 min||water bath||microscopy||water||?||Goheen & McGrew (1954)|
|P. penetrans||strawberry roots||inoculum||49 const|| 7·5 min||water bath||microscopy||water||?||Goheen & McGrew (1954)|
Table 9. Temperature–time conditions for survival of plant-parasitic nematodes in compost and other systems
|Heterodera schachtii||cysts||biowaste||50 max||40 h||heap||larval emergence||ZnCl2 soln||Rykeboer (2001)|
|In other systems|
|Globodera pallida||cysts||sludge||35 av||10 days||anaerobic digester||larval emergence||diffusate||Turner et al. (1983)|
|Heterodera schachtii||cysts||biowaste||52 const||30 min||anaerobic digester||larval emergence||ZnCl2 soln||Ryckeboer et al. (2002a)|
|Meloidogyne javanica||potato tubers||inoculum||47·5 const||1 h||water bath||bioassay||tomato||Martin (1968)|
|Meloidogyne hapla||rose roots||inoculum||44·5 const||2 h||water bath||larval emergence||rose||Martin (1968)|
|M. hapla||rose roots||inoculum||45·5 const||30 min||water bath||larval emergence||rose||Martin (1968)|
|M. hapla||strawberry roots||inoculum||44 const||1 h||water bath||microscopy||water||Goheen & McGrew (1954)|
The times quoted for eradication depend on the intervals used for retrieving samples for viability testing. In some cases, the first retrieval was not until 3 or more weeks after the start of the test (e.g. Bollen et al., 1989) so that a shorter eradication time cannot be specified.
The pathogen inocula for composting tests were normally infected plant materials. These may have contained a single type or a range of types of growth stages or propagules. In some work, the growth stage or propagule used for inoculum is specified (e.g. spores, sclerotia, mycelium). In all the references, the viability of the uncomposted inoculum (positive control treatment) was confirmed with the same procedure used for testing the viability of inoculum retrieved from the compost.
The apparent eradication of a pathogen can be an artefact of the experimental system. In most references only a single population size of test organism was used in eradication tests. Given that the survival time for individual propagules will not be the same for each individual, but will follow some type of statistical distribution for a given set of conditions and detection assay, the apparent survival will vary according to initial population size. For example, Jones (1982) showed that the initial population of Salmonella propagules was positively related to the survival rate at different temperatures. Thus variation in the initial populations may (at least partly) explain differences in eradication test results between different authors.
Methods used for assessing survival of plant pathogens and nematodes during composting
In order to assess the survival of plant pathogens in compost, some method for recovering the target pathogen from the composted material is required. In nearly all the papers reviewed, this was achieved by placing inoculum in nylon sacks or some other inert container, which was then withdrawn from the compost either at the end of, or at intervals during, the composting process. Once retrieved, the material was assayed for the presence of the pathogen. The methods used to assay the recovered samples are indicated in Tables 2–9, and included bioassays, direct plating, dilution plating, serological and direct microscopic examination.
Detection limits and reliability
Associated with any assay is a limit of detection (the lowest concentration that can be detected with a reasonable statistical certainty) and/or a limit of quantification (the lowest concentration that can be determined with acceptable precision and accuracy). Assays may also be subject to other errors and variability, and the final results and their interpretation are subject to sampling errors.
In order to assess the reliability and value of negative results from detection assays, it is vital to have some estimate of the detection limits (or analytical sensitivity). In the majority of the papers reviewed, the authors provided no information and did not appear to have considered this aspect of their work. Therefore, wherever possible, an attempt was made to derive estimates for theoretical detection limits based on the information provided in the papers, and these are given in the appropriate tables for a probability of 0·95: a negative result means that 19 times out of 20 the amount of pathogen will be at this value or below. However, in many cases it was impossible to establish meaningful values due to lack of sufficient detail about the assay method or the numbers of test plants.
Detection of fungi, plasmodiophoromycetes and oomycetes
In addition to true fungi, this review includes several plasmodiophoromycetes (Plasmodiophora brassicae and Polymyxa betae) and oomycetes (Pythium and Phytophthora spp.). Bioassays were the most commonly used method for the detection of fungal pathogens (Tables 2–4). In these bioassays, susceptible indicator plant species were grown in samples of the test compost in pots. In some cases the test material was mixed or diluted with a quantity of sterile soil or compost containing fertilizers, lime, etc. to ensure satisfactory plant growth and to avoid problems with toxicity of the fresh compost. Seeds of susceptible indicator species were then either sown directly into the compost or compost mix, or young plants were transplanted. Following incubation for periods of up to several weeks, the presence of particular disease symptoms on plants was taken to indicate the presence of the pathogen.
The success of such bioassays depends critically on the expression of typical disease symptoms in the indicator species. This means that the environment and indicator need to be selected carefully, but there is little evidence that these aspects have been well researched. In the case of Rhizoctonia solani (Christensen et al., 2001), indicator plants, although infected, did not express symptoms, as demonstrated by a subsequent serological test on the indicator plants. Other subtle details of an assay may also affect the reliability of the results. For example, Lopez-Real & Foster (1985) stored recovered samples at −24°C before assay, but there is no indication of whether or not this could have had an effect on the viability of pathogen propagules.
None of the papers reviewed gave a clear indication of the analytical sensitivity or recovery rate. Detection limits were calculated as the minimum proportion of infected plants that can be detected with a probability of 0·95, on the basis of the numbers of plants evaluated and assuming a binomial model for infection (Roberts et al., 1993). These are expressed in Tables 2–9 as ‘% inf’ and necessarily assume that recovery is 100%. Where the proportion of plants infected in the positive control treatments was less than 100%, then the detection limit must be greater than the theoretical minimum and this is indicated by a greater than sign (>) in the tables.
The sensitivity or recovery of soilborne pathogens by bioassays has been reported only occasionally: 103 spores g−1 peat and 106 spores g−1 soil for P. brassicae (Staniaszek et al., 2001) and 1·7% recovery for P. betae (Tuitert, 1990).
Direct plating or dilution plating was used for some of the culturable fungi (Tables 2–4). Pieces of composted plant residue or recovered propagules were placed directly on the surface of agar plates, which were then incubated and observed for outgrowth of mycelium or sporulation. Estimates of detection limits were calculated as the proportion of residue containing viable pathogen or the proportion of propagules remaining viable on the basis of the number of residue pieces/sclerotia/spores evaluated and assuming a binomial model. Agar and potato dextrose agar (PDA) were the most commonly used media, although prune–lactose–yeast (PLY) agar (Talboys, 1961), selective agars, and other plant-based media were also used.
Baiting and plating was used by Hoitink et al. (1976) for Pythium and Phytophthora spp. Lupin seedlings were used as the bait to attract zoospores in a water extract of the soil/compost and after incubation (e.g. overnight) the seedlings were plated on a selective agar medium.
In common with DNA-based methods, serological methods cannot distinguish between viable and dead cells, and therefore may not be appropriate to indicate disease risks from composts. However, serological methods such as enzyme-linked immunosorbent assay (ELISA) have been used as a secondary confirmation step following baiting of test plants (Christensen et al., 2001) (Tables 2 and 3).
Detection of bacteria
Bioassays were used to detect bacterial pathogens in only one of the papers examined, where crude extracts of composted material were injected directly into host plants (Lopez-Real & Foster, 1985). Insufficient data were provided to allow estimation of detection limits.
Dilution plating was the most common method used for bacteria (Table 5). Samples of residue were macerated, then diluted and spread on the surface of selective agar plates. If suitable selective media are available which inhibit the growth of more rapidly growing saprophytes, plating can be a very sensitive method for detection. However, if plating is done on nonselective media the results can be unreliable due to overgrowth of saprophytes masking the presence of the target pathogen. Selective media used in the tests were Miller–Schroth (M-S) (Bruns et al., 1993); D2 broth (Turner et al., 1983), King's medium B, supplemented with cycloheximide (Keck et al., 1995), and a selective agar prepared for Ralstonia solanacearum (Ryckeboer et al., 2002a).
Although it is relatively easy to estimate (theoretical) detection limits for dilution plating assays, in most cases insufficient data were provided to allow this. Where theoretical values are given it is likely that the practical sensitivity is poorer due to interference from saprophytes. The data from Hoitink et al. (1976) allowed estimation of limits in terms of the proportion of residue assuming 100% recovery.
Detection of viruses
All of the virus pathogens were detected by bioassays (Tables 6 and 7). In most of these bioassays, samples of composted material were suspended in buffer, which was then used for direct inoculation of an indicator plant. In some cases (Avgelis & Manios, 1989) the extract was centrifuged and then resuspended in a smaller volume to increase the virus concentration before inoculation (that is, to increase sensitivity). If the virus is present the indicator plant, often a Nicotiana species, produces characteristic symptoms of the virus, usually local lesions, within 7–14 days. The number of lesions can be used to provide a relative estimate of the number of virus particles in the sample extract. Sometimes (e.g. Ryckeboer et al., 2002a) the test extract was applied to one half of a leaf and a positive control (e.g. uncomposted material) was applied to the other half, following the method suggested by Walkey (1991). Some authors (Christensen et al., 2001; Suarez-Estrella et al., 2002) also performed a secondary ELISA test on extracts of the inoculated leaves to confirm the presence of the virus in inoculated leaves. It was impossible to make meaningful estimates of the detection limits of these assays. Even where other details were provided, the volume of extract applied to the leaves was not recorded or estimated, and the efficiency of extraction was unknown.
Where the virus is transmitted by a vector such as Olpidium brassicae (e.g. Tobacco necrosis virus, TNV; Asjes & Blom-Barnhoorn, 2002 or Lettuce big vein virus, LBVV; Coventry et al., 2002), or is considered to survive in debris (e.g. Cucumber green mottle mosaic virus, CGMMV; Avgelis & Manios, 1992), the bioassay was performed by planting susceptible hosts into the material in the same way as for soilborne fungal pathogens. In these cases the detection limits were estimated as a proportion of test plants infected, as for the fungi.
A major advantage of bioassays for viruses is that only infective virus particles are detected, whereas the direct use of a serological or molecular method may detect noninfectious virus particles.
Detection of nematodes
Survival of nematodes was assessed either by bioassay or by counting the number of larvae or juveniles emerging from eggs or cysts (Tables 8 and 9). The emergence of juveniles was usually stimulated by diffusates or ZnCl2 solution. The bioassays were performed in a similar way to those for soilborne fungi, with indicator plants grown in admixtures of the composted material. Detection limits were therefore estimated as the proportion of test plants infected. Larval emergence counts were done by direct microscopic observation of the number of juveniles or larvae emerging from cysts or eggs. Detection limits were therefore estimated as the proportion of cysts or eggs surviving.
Temperature–time effects on plant pathogens and nematodes
Data on temperature–time effects and other sanitizing factors of composting on the eradication and/or survival of 64 plant pathogens and nematodes was retrieved from 52 publications. Of these species and subspecies or pathovars, 47 were examined in compost and 17 were only examined in plant material (with dry heat or steam–air), soil, agar, water or anaerobic digester liquid. Most workers determined a single temperature and time, or limited combinations of temperature and time, for eradication of plant pathogens during composting or in other systems. Feacham et al. (1983) determined the effect of combinations of temperature and time in composting sewage sludge on the eradication of several animal pathogens, including Salmonella spp. and Acaris nematodes. In their tests, as compost temperature declined from 65 to 40°C, eradication times increased from < 1 h to > 100 h. The effects of multiple combinations of temperature and time on eradication have been examined on only a small number of plant pathogens, and usually in noncomposting systems, e.g. for P. ultimum, Verticillium spp. and Thielaviopsis basicola (Talboys, 1961; Pullman et al., 1981). Similarly to the above work on animal pathogens, this work has shown a logarithmic relationship between the time required for eradicating a pathogen and the temperature. More comprehensive data are required before comprehensive temperature–time matrices for the eradication of particular plant pathogens or nematodes from composting feedstocks can be constructed.
Plant pathogens (fungi, oomycetes and plasmodiophoromycetes)
Of the 25 fungal pathogens examined in compost, 20 were eradicated and Fusarium oxysporum f.sp. pisi was reduced to values very close to the detection limit after 7 days in compost at 50°C (Table 3). Lower peak or constant temperatures and/or shorter durations may have been satisfactory for eradication, but they were rarely examined in detail in composting systems. Tests in other, noncomposting systems showed that a further eight fungal pathogens were eradicated by a temperature of 55°C held for 14 days or less, although Synchytrium endobioticum, the causal agent of potato wart disease, survived in water at 60°C for 2 h (eradicated after 8 h, Table 4) (Glynne, 1926).
Fusarium oxysporum f.sp. lycopersici, the causal agent of tomato wilt, survived a peak compost temperature of at least 65°C (possibly as high as 74°C), and a composting duration of up to 21 days, using infected kernels as inoculum (Christensen et al., 2001) (Table 3). Fusarium oxysporum f.sp. melongenae also survived a 21-day composting period with a peak temperature of 53–65°C. These F. oxysporum formae speciales were not examined at constant temperature, or in other systems. Although F. oxysporum f.sp. pisi survived composting at 50°C for 7 days (Table 3), it was reduced to levels close to the detection limit, and can therefore be assumed to be more temperature-sensitive than the above formae speciales. Other F. oxysporum formae speciales also appeared to be less temperature-tolerant than F. oxysporum f.sp. lycopersici when tested by other workers (Tables 2 and 4). F. oxysporum f.sp. narcissi was eradicated after composting for 7 months, even though compost temperatures did not exceed 40°C (Table 2).
The pathogen that causes dry root rot of beans and other crops in warm climates, Macrophomina phaseolina, was also able to survive a peak compost temperature of 60–62°C, and a composting duration of up to 21 days (Lodha et al., 2002). Conditions for eradicating this pathogen from compost were not established.
Tests in compost (Table 2) and using dry heat (Table 4) showed that sclerotia of Sclerotinia sclerotiorum required peak temperatures of up to 74°C for up to 23 days for eradication. Tests in soil at controlled temperature (van Loenen et al., 2003) (Table 4) showed that S. sclerotiorum was eradicated at 60°C for 3 min. Sclerotia of Sclerotinia fructigena, Sclerotinia minor, Sclerotium cepivorum and Sclerotium (Corticium) rolfsii were all sensitive to constant temperatures below 55°C in compost or other media (Tables 2 and 4).
One Pythium and four Phytophthora species were eradicated in compost heaps that reached peak temperatures of 64–70°C during 21 days, or 50°C during 77 days (Table 2). Tests in noncomposting systems showed that these pathogens, as well as P. ultimum, were eradicated by a temperature of 55°C held for 14 days or less (Table 4). Bollen et al. (1989) found a very low level of survival of O. brassicae, the vector of LBVV and TNV, at composting temperatures of 56–67°C, i.e. one test plant out of 53 had a few viable spores in one of the 20 roots examined (Table 3). Single sporangial isolates of O. brassicae were eradicated after 10 min in water at 50°C (Table 4), although there was survival of resting spores in root material (Campbell & Lin, 1976).
Data obtained for P. brassicae, the causal agent of clubroot of Brassica spp., were very variable. Lopez-Real & Foster (1985), Bollen et al. (1989), and Ryckeboer (2001) found that a peak temperature of 54–60°C and composting duration of 1–21 days eradicated the organism. Christensen et al. (2001) eradicated P. brassicae by using an average compost temperature of 49°C for 14 days (Table 2). However, Ylimaki et al. (1983) and Bruns et al. (1993) showed that peak temperatures of 60–80°C and composting durations of 49 days or longer were required for eradication (Tables 2 and 3). Water-bath tests (Table 4) also showed that temperatures over 75°C were required for eradication of P. brassicae in filtered suspensions, although the tests were conducted for only 10 min (Lopez-Real & Foster, 1985). Both Bollen et al. (1989) and Ryckeboer et al. (2002b) demonstrated that P. brassicae could survive for long periods at lower temperatures during the maturation phase of composting. Experiments described by Sansford (2003) indicated that P. betae, the vector of Beet necrotic yellow vein virus (BNYV), was eradicated by a composting temperature of 60°C for 1 day, but there was some survival of spores in soil/water suspensions held at 75°C for 30 min.
Bacterial plant pathogens
There is less published information on the eradication conditions for bacterial plant pathogens compared with that for fungi and viruses, and only four bacterial plant pathogens have been examined in composting systems. All the bacterial plant pathogens in Table 5 could be eradicated by a temperature of 60°C, although some contradictions are apparent. For example, Keck et al. (1995) found that Erwinia amylovora was eradicated in apple budwood subjected to dry heat for 3 h at 45°C, but not when subjected to moist heat at 50°C for the same period. This result is odd because bacteria are usually killed more effectively by moist heat than dry heat (e.g. Turner, 2002). It is possible that such contradictions are entirely due to the limited numbers of experimental units examined in the experiments, (e.g. 35 experimental units give a reliable detection limit of approximately 9%).
The regrowth of Salmonella spp. in compost is possible in some circumstances (Russ & Yanko, 1981; Burge et al., 1987). The risks of regrowth of bacterial plant pathogens in composted plant debris have not been examined.
Viral plant pathogens
Bartels (1955) reviewed and Walkey & Freeman (1977) examined the inactivation by heat of a range of viruses in plant material that survived the heat treatment. However, this information cannot be extrapolated to the composting situation, as living plant tissue may have an independent effect on viral inactivation.
Coventry et al. (2002) and Asjes & Blom-Barnhoorn (2002) showed the infectivity of the LBVV/Olpidium and TNV/Olpidium complexes was eliminated by composting at 50°C for 7 and 50 days, respectively (Table 6). Melon necrotic spot virus, TNV and Tomato spotted wilt virus could be eradicated by a peak composting temperature of 65°C and a composting duration of up to 28 days (Table 6). CGMMV, Pepper mild mottle virus, Tobacco mosaic virus (TMV) and Tobacco rattle virus were more temperature-tolerant (Tables 6 and 7). Eradication conditions for TMV were variable, but Price (1933); Hoitink & Fahy (1986); Hermann et al. (1994) and Christensen et al. (2001) found that peak temperatures over 66°C and composting periods of longer than 28 days were needed. Ryckeboer (2001) also found that a peak compost temperature of 78°C and duration of 57 days was required for eradication, but TMV did not survive after a long period in compost (26 weeks), even at low temperature (31°C) (Table 6). For TMV, microbial degradation of infected plant tissue and virus particles during composting may therefore be more important in achieving eradication than temperature–time effects. The same may apply to Tomato mosaic virus (TomMV), which remained viable in tomato seeds after heating at 70°C in an incubator for more than 20 days (Broadbent, 1965; Howles, 1961), but was inactivated in composted tomato plants after 10 days with a maximum temperature of 46°C (Avgelis & Manios, 1989). However, it should be noted that the detection limit in the latter work was poor.
Infected seeds in compost may be a possible source of TMV and TomMV inoculum. Hermann et al. (1994) reported destruction of tomato seeds in compost in 3–4 days at temperatures of 55–65°C. Christensen et al. (2002) also found that tomato seeds became soft and were no longer viable after exposure to a compost temperature of 60°C for 10 days.
Plant pathogenic nematodes
All of the nematode species in Table 8 were eradicated by a constant or average compost temperature of 60°C, and a composting duration of < 2 days, with the exception of beet cyst nematode (Heterodera schachtii). The cysts had the ability to survive in compost for up to 6 months of the maturation phase (Ryckeboer et al., 2002b), but were readily killed during the sanitization phase (Table 8). The root knot nematode Heterodera marioni (possibly a synonym of Meloidogyne hapla) declined markedly during a 20-week period when decomposing plant waste was added to soil containing galls, but there was no decline of viable galls in the soil alone, although temperatures did not exceed 27°C (Linford et al., 1938). This indicates that microbial antagonism and/or degradation of the host plant material are important in the eradication of plant parasitic nematodes from decomposing plant wastes.
Insect pests, such as the larvae of Narcissus bulb fly (Merodon equestris) and mushroom cecid fly (Heteropeza pygmaea) are sensitive to a temperature of 45°C (Becker, 1974; Fletcher et al., 1989). Coventry et al. (2001) found that onion fly larvae (Delia antiqua) were eradicated from onion waste by composting at 50°C for 1 day (lower temperatures and shorter times were not examined).
Other compost factors involved in pathogen eradication
The moisture content of the organic waste can influence the temperature tolerance of microorganisms, and the occurrence of dry pockets in composting material is probably the main cause of pathogen survival in heaps where eradication was expected on the basis of compost temperatures (Bollen & Volker, 1996). These workers recommended a minimum compost moisture content of 40%. However, the effect of compost moisture on the thermal sensitivity of plant pathogens has not been studied in detail.
The pH may influence pathogen survival if composting conditions are very acidic or alkaline, but this is unlikely to occur under normal composting conditions (Christensen et al., 2002). In reviews by Bartels (1956) and Hermann et al. (1994), pH values between 3 and 8 did not inactivate S. sclerotiorum or TMV, and values between 5·5 and 8 did not inactivate nematodes.
It is known that some mycelial plant pathogens (e.g. Phytophthora cinnamomi, S. rolfsii) are killed after exposure to relatively high concentrations of ammonia (Henis & Chet, 1968; Gilpatrick, 1969). In the first stages of composting crop residues rich in nitrogen, ammonia probably contributes to sanitization (Bollen & Volker, 1996). Toxic products formed under anaerobic conditions, such as organic acids, may affect pathogens during composting (Bollen & Volker, 1996). Ryckeboer et al. (2002a) found that P. brassicae was sensitive to temperature in anaerobic digester liquid (Table 4), whereas this organism was temperature-tolerant under aerobic composting conditions (Table 3).
The temperature required to eradicate Escherichia coli depended on the composting feedstocks used (Turner, 2002). Differences in moisture or ammoniacal nitrogen did not account for these differences in eradication temperature, although eradication was improved by higher moisture content within a particular feedstock. There is little information on the independent effect of composting feedstocks on the eradication of plant pathogens. The improved eradication of S. sclerotiorum in heaps of composting green waste/manure compared with that in heaps of green waste/straw is consistent with the higher temperatures achieved in the former (Dittmer et al., 1990).
The microbial degradation of infected plant material in compost has already been mentioned. Microbial antagonism is one of the principal factors involved in disease suppressive properties of compost (Hoitink & Boehm, 1999). However, the role of microbial antagonism in the destruction of pathogens in compost heaps has not been established experimentally (Bollen & Volker, 1996).
Temperature profiling of commercial composting systems
The following are listed by Rynk & Richard (2001) as the main categories of composting system: (i) turned windrows; (ii) passively aerated static piles; (iii) forced aerated static piles; (iv) combined turned and forced aerated windrows; (v) in-vessel systems (horizontal agitated beds, aerated containers or ‘tunnels’, aerated-agitated containers, silo or tower reactors).
The effectiveness of different composting systems in reducing the pathogen content of the compost products has been examined by de Bertoldi et al. (1988); Stentiford (1996); Christensen et al. (2001, 2002). This work has shown that maintaining adequate aeration to provide oxygen for thermophilic microorganisms, without hyperventilation, is important in achieving sufficiently high temperatures for sanitization of compost. In turned windrows without aeration, the interior of the stack becomes depleted of oxygen soon after turning (Day & Shaw, 2001), and 10–20% of the composting mass may become anaerobic (Miller et al., 1991). Standards for compost sanitization have been developed in the USA by the Composting Council of the United States (Leege & Thompson, 1997), in the UK jointly by the Waste and Resources Action Programme (WRAP) and the Composting Association (Anon, 2002), as well as in several other European countries (Stentiford, 1996). These specify minimum compost temperatures of 55–65°C for periods of 3–14 days depending on the composting system (turned windrow, in-vessel, static aerated piles). A risk assessment of composting to dispose of catering waste containing meat recommended a minimum composting temperature of 60°C for 2 days (Gale, 2002). Based on survival probabilities, this report also recommended that windrows should be turned at least three times and the composting process should last at least 14 days. Christensen et al. (2002) recommend even more stringent sanitary requirements: 70°C for 2 days or 65°C for 4 days, with at least five turnings in windrow systems.
Most references referring to temperature during composting show mean or maximum temperatures achieved. However, of critical importance for pathogen eradication is the proportion of the compost that remains below the specified sanitization standards. This will depend on the composting system, its management, the ambient temperatures, and the quantity and type of feedstocks used. Much of the previous work on temperature profiling of composting systems relates to the eradication of animal pathogens, and has been conducted with compost activators such as sewage sludge or animal manures. Of greater relevance to the eradication of plant pathogens are temperature profiles of composting plant residues that may be low in available nitrogen and other nutrients.
Temperatures above 60°C were achieved in all the composting tests in Table 2, except with hardwood bark waste with inorganic fertilizer (Hoitink et al., 1976), spice–sawdust mix (Yuen & Raabe, 1984), green waste mixed with straw (Dittmer et al., 1990), and bulb peelings waste (Bollen et al., 1991). There were often compost temperature ranges of 20°C or higher within composting systems. However, probability studies (Gale, 2002) have shown that the risk of pathogen survival in windrow systems is small, provided the windrows achieve the stipulated average temperatures and are turned at least the specified minimum number of times. Of greater concern for pathogen survival are the cool zones in static and in-vessel composting systems where there is no or little turning. Data sets analysed by Gale (2002) indicate that, of the composting green waste in turned-windrow and in-vessel systems, at least 20 and 5%, respectively, is below 55°C at any particular time. However, measurements by Christensen et al. (2001, 2002) show that there are significant differences in spatial and temporal temperature profiles between different windrow and in-vessel composting facilities. Further work is needed to determine whether the eradication conditions for temperature-tolerant plant pathogens such as P. brassicae and some F. oxysporum formae speciales can be achieved consistently in different composting systems using plant-based feedstocks.
- • Bioassays were the most frequently used methods for the detection of plant pathogenic fungi, oomycetes and viruses, whereas dilution plating was most frequently used for bacterial pathogens.
- • It is clear that the detection limits in most studies were quite poor, with infection levels of up to 5% likely to be undetected regularly, and this may explain the variable or inconsistent results obtained for some pathogens by different authors. In most cases it is therefore difficult to determine the value of the results in terms of a quantitative assessment of the risk of using composted wastes for crop production, especially where many thousands of plants could be grown in a batch of compost.
- • Experimental designs and detection assays should consider the likely end-user requirements in terms of acceptable infection risk. In current horticultural practice, even 1% primary infection is likely to be unacceptable, and this detection limit was not achieved in any of the composting studies. An essential part of any further work on the eradication of plant pathogens in compost should be to determine the practical recovery and detection limits of the assay used.
- • The temperature–time eradication conditions of 64 plant pathogen and nematode species have been retrieved from the literature. For 27 out of 32 pathogenic fungi, all six oomycetes, seven bacterial pathogens and nine nematodes, and three out of nine plant viruses, a peak temperature of 64–70°C and duration of 21 days were sufficient to reduce numbers to below, or very close to, the detection limits of the tests used. In many of the references, the temperatures and times required for eradication have not been determined precisely. Shorter periods and/or lower temperatures may therefore be satisfactory.
- • The fungal pathogens F. oxysporum f.sp. lycopersici (tomato wilt) and M. phaseolina (dry root rot) and the clubroot pathogen P. brassicae were more temperature-tolerant as they survived a peak compost temperature of at least 62°C (maximum 74°C) and a composting duration of 21 days. The plasmodiophoromycete P. betae was eradicated by this treatment, but survived in soil/water at 75°C for 30 min. The fungal pathogen S. endobioticum (potato wart disease) survived in water at 60°C for 2 h (eradicated after 8 h), but was not examined in compost.
- • Several plant viruses were temperature-tolerant. These were CGMMV, Pepper mild mottle virus, Tobacco rattle virus, ToMV and TMV. TMV requires a peak compost temperature in excess of 68°C and a composting period longer than 20 days for eradication. However, TMV is degraded in compost over time, and can be eradicated after a composting period of 26 weeks, even at low temperature (31°C). ToMV in infected seeds can withstand over 70°C in an incubator for over 20 days.
- • There are insufficient data to produce comprehensive temperature–time matrices for the eradication of particular plant pathogens during composting, as has been achieved for some animal pathogens.
- • Maximum compost temperatures above 60°C were achieved in different composting systems with a wide range of feedstocks. However, there were often compost temperature ranges of 20°C or higher within composting systems. This is of particular importance in static or enclosed in-vessel systems where there is no turning of the wastes, and sanitization may be incomplete.
This review was funded by the Waste and Resources Action Programme (WRAP), Banbury, Oxon, UK and the European Union as part of project QLRT-2000-01458 ‘RECOVEG’. The authors acknowledge helpful input and criticism from Dr JT Fletcher, Professor JM Whipps, Ms E Nichols, Ms L Hollingworth and Dr A Rainbow.