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Keywords:

  • compost;
  • sanitization;
  • survival;
  • temperature

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Systems used for studying temperature–time effects on eradication
  5. Methods used for assessing survival of plant pathogens and nematodes during composting
  6. Temperature–time effects on plant pathogens and nematodes
  7. Other compost factors involved in pathogen eradication
  8. Temperature profiling of commercial composting systems
  9. Conclusions
  10. Acknowledgements
  11. References

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.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Systems used for studying temperature–time effects on eradication
  5. Methods used for assessing survival of plant pathogens and nematodes during composting
  6. Temperature–time effects on plant pathogens and nematodes
  7. Other compost factors involved in pathogen eradication
  8. Temperature profiling of commercial composting systems
  9. Conclusions
  10. Acknowledgements
  11. References

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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Systems used for studying temperature–time effects on eradication
  5. Methods used for assessing survival of plant pathogens and nematodes during composting
  6. Temperature–time effects on plant pathogens and nematodes
  7. Other compost factors involved in pathogen eradication
  8. Temperature profiling of commercial composting systems
  9. Conclusions
  10. Acknowledgements
  11. References

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
PathogenHost(s)Common name of disease or nematode
Fungi
Armillaria melleavarious woodyhoney fungus
Botrytis aclada (syn. allii)onion (Allium cepa)neck rot
Botrytis cinereavariousgrey mould
Colletotrichum coccodesSolanaceaeanthracnose
Didymella lycopersicitomato (Lycopersicon esculentum)stem rot
Fusarium oxysporum f.sp. callistephiAster spp.wilt
F. oxysporum f.sp. dianthicarnation, pink (Dianthus spp.)wilt
F. oxysporum f.sp. liliilily (Lilium spp.)scale rot
F. oxysporum f.sp. lycopersicitomato (L. esculentum)wilt
F. oxysporum f.sp. melongenaeegg plant (Solanum melongena)wilt
F. oxysporum f.sp. melonismelon (Cucumis melo)wilt
F. oxysporum f.sp. narcissiNarcissus spp.basal rot
F. oxysporum f.sp. pisipea (Pisum sativum)wilt
Fusarium solani f.sp. cucurbitaeCucurbitaceaewilt
Macrophomina phaseolinavariousdry root rot
Olpidium brassicaevariousvectors of LBVV and TNV
Phomopsis sclerotioidescucumber (Cucumis sativus)black rot
Pseudocercosporella herpotrichoideswheat (Triticum aestivum)foot rot
Pyrenochaeta lycopersicitomato (L. esculentum)corky root
Rhizoctonia solanivarious potato black-scurfdamping-off,
Sclerotinia fructigenastone fruits (Prunus spp.)brown rot
Sclerotinia minorvariousblight
Sclerotinia sclerotiorumvariouswatery soft rot
Sclerotium cepivorumAllium spp.white rot
Sclerotium (Corticium) rolfsiivarioussouthern blight
Septoria lycopersicitomato (L. esculentum)leaf spot
Stromatinia gladioliGladiolus spp.dry rot
Synchytrium endobioticumpotato (Solanum tuberosum)wart disease
Taphrina deformanspeach (Prunus persica)leaf curl
Thielaviopsis basicolavariousblack root rot
Verticillium albo-atrumhop (Humulus lupulus)wilt
Verticillium dahliaevariouswilt
Plasmodiophoromycetes
Plasmodiophora brassicaeBrassicaceaeclubroot
Polymyxa betaeChenopodiacaevector of BNYV
Oomycetes
Phytophthora cinnamomivariousroot rot, dieback
Phytophthora cryptogeavariouscollar rot, root rot
Phytophthora infestanspotato (S. tuberosum)potato blight
tomato (L. esculentum) 
Phytophthora ramorumvarious woodysudden oak death
Pythium irregularevariousroot rot
Pythium ultimumvariousdamping-off, root rot
Bacteria
Clavibacter michiganensis ssp. michiganensistomato (L. esculentum)canker
Erwinia amylovoraRosaceaefire blight
Erwinia carotovora ssp. atrosepticapotato (S. tuberosum)black leg and soft rot
Erwinia carotovora ssp. carotovoravarioussoft rot
Erwinia chrysanthemivarioussoft rot, blight
Pseudomonas savastanoi pv. phaseolicolaPhaseolus beans 
Ralstonia solanacearumSolanaceaebacterial wilt
Viruses (abbreviation)
Cucumber green mottle mosaic (CGMMV)cucumber (Cucumis sativus) 
Lettuce big vein (LBVV)lettuce (Lactuca sativa) 
Melon necrotic spotCucurbitaceae 
Pepper mild mottleSolanaceae 
Tobacco mosaic (TMV)various 
Tobacco necrosis (TNV)various 
Tobacco rattle (TRV)various 
Tomato mosaic (ToMV)various 
Tomato spotted wilt virusvarious 
Nematodes
Aphelenchoides ritzemabosiChrysanthemum spp. strawberry (Fragaria spp.) 
Globodera pallidapotato (S. tuberosum),white potato cyst
tomato (L. esculentum) 
Globodera rostochiensispotato (S. tuberosum),yellow potato cyst
tomato (L. esculentum) 
Heterodera schachtiibeet (Beta vulgaris)beet cyst
Meloidogyne chitwoodiivariousroot-knot
Meloidogyne haplapotato (S. tuberosum)northern root-knot
Meloidogyne incognitabeet (B. vulgaris)southern root-knot
Meloidogyne javanicavariousJavanese root-knot
Pratylenchus penetransstrawberry (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
PathogenInoculumFeedstock (in heaps unless stated)Temperaturea (°C; max unless stated)Time (days)DetectionReference
MethodMediumLimitb
  • a

    Maximum, average or constant temperatures recorded.

  • b

    Detection limit estimated from experimental details for P = 0·95 as percentages of test plants infected (% inf), residue samples tested (% res), sclerotia surviving (% scler), or not determined or stated (?).

Fungi
Armillaria melleacherry woodgarden refuse70 21platingPDA12% resYuen & Raabe (1984)
Botrytis acladabulbs/sclerotiagarden refuse64–70 21bioassayonion bulbs5% infBollen et al. (1989)
Botrytis cinereabean leavesgrass, hop waste, manure35  4bioassaybean?Lopez-Real & Foster (1985)
B. cinereageranium stems/leavesbark60 91platingselective agar4% resHoitink et al. (1976)
Colletotrichum coccodestomato, aubergine roots/stemsgarden refuse64–70 21bioassayaubergine5% infBollen et al. (1989)
Didymella lycopersicitomato haulmsinoculum59–73  7bioassaytomato8% infPhillips (1959)
Fusarium oxysporum
f.sp. callistephiChinese astergarden refuse47–65 21bioassayChinese aster8% infBollen et al. (1989)
f.sp. liliilily bulbsgarden refuse58–70 21bioassaylily bulb scales> 3% infBollen et al. (1989)
f.sp. melonismelon roots/stemsgarden refuse56–67 21bioassaymelon4% infBollen et al. (1989)
f.sp. melonismelon residueplant residues64  4platingPDA?Suarez-Estrella et al. (2003)
f.sp. narcissibulb peelingsplant residues40210???Bollen et al. (1991)
Fusarium solani f.sp. cucurbitaecourgette roots/stemsgarden refuse53–65 21bioassaycourgette8% infBollen et al. (1989)
Phomopsis sclerotioidesgherkin rootsgarden refuse64–70 21bioassaygherkin> 4% infBollen et al. (1989)
Pseudocercosporella herpotricoidesmyceliumgreen waste, straw60  7platingwater agar + antibiotics?Dittmer et al. (1990)
Pyrenochaeta lycopersicitomato rootsgarden refuse53–65 21bioassaytomato5% infBollen et al. (1989)
Rhizoctonia solanipotato tubers/sclerotiagarden refuse64–70 21bioassaypotato> 13% infBollen et al. (1989)
R. solanimillet seedgarden refuse, sawdust70 21platingwater agar12% resYuen & Raabe (1984)
R. solanibeet piecesbark50 77bioassaybeet2% infHoitink et al. (1976)
R. solaniwheat kernelshousehold, various52 av 49bioassay + ELISAbean> 9% inf Christensen et al. (2001)
Sclerotinia sclerotiorumlettuce stems/sclerotiagarden refuse64–70 21bioassaycucumber> 5% infBollen et al. (1989)
S. sclerotiorumsclerotiagreen waste, manure74 23fluorescence microscopefluorescein diacetate5% sclerDittmer et al. (1990)
S. sclerotiorumsclerotiabiowaste74 18platingPDA?Hermann et al. (1994)
Sclerotium cepivorumbulbs/sclerotiagarden refuse64–70 21bioassayonion> 8% infBollen et al. (1989)
S. cepivorumsclerotiaonion waste (flasks)48 const  3platingPDA2% sclerCoventry et al. (2002)
Sclerotium rolfsiisclerotiaspice–sawdust32 12platingwater agar2% sclerYuen & Raabe (1984)
Stromatinia gladioligladiolus leaves/sclerotiagarden refuse64–7021bioassaygladiolus2% infBollen et al. (1989)
Thielaviopsis basicolaspores?63?heap??Grushevoi & Levykh (1940)
Verticillium dahliaerose stemsgarden refuse, sawdust7021platingcellophane agar20% resYuen & Raabe (1984)
Plasmodiophoromycetes
Plasmodiophora brassicaecabbage rootsgarden refuse47–6521bioassayChinese cabbage> 8% infBollen et al. (1989)
P. brassicaecabbage rootsgrass, hop waste, manure54 av 1bioassaycabbage?Lopez-Real & Foster (1985)
P. brassicaegalls/soilhousehold, woodchips60–8049bioassaycauliflower9% infBruns et al. (1993)
P. brassicaegalls/soilhousehold, various49 av14bioassayBrassica juncea> 7% infChristensen et al. (2001)
P. brassicaecauliflower roots/soilbiowaste or green waste60 av 2bioassayBrassica juncea?Ryckeboer (2001)
Oomycetes
Phytophthora cinnamomirhododendron crown/rootsbark5077baiting + platinglupin?Hoitink et al. (1976)
Phytophthora cryptogeaChinese aster root clodsgarden refuse64–7021bioassayChinese aster> 5% infBollen et al. (1989)
Phytophthora infestanspotato tubersgarden refuse47–6521bioassaypotato disks3% infBollen et al. (1989)
Phytophthora ramorumoak wood, laurel leaveswood chips, green waste?14bioassaypear?Garbelotto (2003)
Pythium irregularerhododendron crown/rootsbark5077baiting + platinglupin?Hoitink et al. (1976)
Table 3.  Temperature–time conditions for survival of plant pathogenic fungi and plasmodiophoromycetes in compost
PathogenInoculumFeedstock (in heaps unless stated)Temperaturea (°C, max unless stated)Time (days)DetectionReference
MethodMedium
  • a

    Maximum, average or constant temperatures recorded.

  • b

    Recorded after the test at values close to the limit of detection.

Fungi
Didymella lycopersicitomato haulmsinoculum56 27bioassaytomatoPhillips (1959)
Fusarium oxysporum
f.sp. lycopersiciwheat kernelshousehold, various74 21bioassaytomatoChristensen et al. (2001)
f.sp. melongenaeaubergine root clodsgarden refuse53–65 21bioassayaubergineBollen et al. (1989)
f.sp. pisimycelium/soilonion waste (flasks)50 const  7platingbkomadaCoventry et al. (2001)
Macrophomina phaseolinainfected rootscrop, weed residues60–62 21platingselective agarLodha et al. (2002)
Olpidium brassicaelettuce root clodsgarden refuse56–67 21bioassayblettuceBollen et al. (1989)
Rhizoctonia solaniwheat kernelshousehold, various57 av 14bioassay + ELISAbeanChristensen et al. (2001)
Sclerotinia sclerotiorumsclerotiagreen waste, straw42 23fluorescence microscopefluorescein diacetateDittmer et al. (1990)
Plasmodiophoromycetes
Plasmodiophora brassicaenaturally presentsludge, manure, feathers70175bioassayBrassica nigraYlimaki et al. (1983)
P. brassicaegalls, soilhousehold, woodchips40–60 98bioassaycauliflowerBruns et al. (1993)
P. brassicaegalls, soilbiowaste60182bioassayBrassica junceaRyckeboer et al. (2002b)
Table 4.  Temperature–time conditions for eradication of plant pathogenic fungi, plasmodiophoromycetes and oomycetes in other systems
PathogenInoculumMediumTemp (°C)TimeSystemDetectionReference
MethodMediumLimita
  • a

    Detection limit estimated from the experimental details for P = 0·95 as percentages of test plants infected (% inf), residue samples tested (% res), sclerotia or sporangia surviving (% scler or % spora), propagules mL−1 (prop mL−1), or not determined or stated (?).

Fungi
Armillaria melleacitrus rootsinoculum417 hsteam–airdirect platingagar18% infMunnecke et al. (1976)
A. melleainfected plantsinoculum4930 minsteam–airdirect platingagar18% infMunnecke et al. (1976)
Botrytis cinereageranium stems/leavesinoculum4021 daysincubatordirect platingPDA, selective agar5% resHoitink et al. (1976)
B. cinereageranium stems/leavesinoculum507 daysincubatordirect platingPDA, selective agar5% resHoitink et al. (1976)
B. cinereasporeswater474 minwaterdirect platingagar0·25% resSmith (1923)
B. cinereasporeswater506 minwaterdirect platingagar0·25% resSmith (1923)
B. cinereaconidiawater6510 minwaterbioassaybean?Lopez-Real & Foster (1985)
Fusarium oxysporumsuspensionsewage353 daysanaerobicenrichmentCzapek Dox and PSA30 prop/mLTurner et al. (1983)
f.sp. dianthi sludge  digesterplating   
f.sp. melonismelon residuesinoculum554 daysincubatorplatingPDA?Suarez-Estrella et al. (2003)
Olpidium brassicaesporangiawater5010 minwater bathbioassaylettuce12·5% sporaCampbell & Lin (1976)
Rhizoctonia solanibarley seedinoculum4049 daysincubatordirect platingPDA and water agar?Hoitink et al. (1976)
R. solanibarley seedinoculum507 daysincubatordirect platingPDA and water agar?Hoitink et al. (1976)
R. solanimyceliumwater507 minwaterdirect platingPDA?Miller & Stoddard (1956)
R. solanimyceliumagar5012 minwater bathdirect platingPDA2% resPullman et al. (1981)
Sclerotinia fructigenainfected plants?52?????Spector (1956)
Sclerotinia minorsclerotiasoil501·5 daysincubatordirect platingsemiselective6% sclerAdams (1987)
Sclerotinia sclerotiorumsclerotiainoculum5039 daysincubatordirect platingPDA?Hermann et al. (1994)
S. sclerotiorumsclerotiainoculum704 daysincubatordirect platingPDA?Hermann et al. (1994)
S. sclerotiorumsclerotiasoil603 minsteam–airdirect platingPDA, semiselective3·5% sclervan Loenen et al. (2003)
S. cepivorumsclerotiasoil408 daysincubatordirect platingPDA1% sclerMcLean et al. (2001)
S. cepivorumsclerotiasoil4512 hincubatordirect platingPDA1% sclerMcLean et al. (2001)
S. cepivorumsclerotiasoil506 hincubatordirect platingPDA1% sclerMcLean et al. (2001)
S. cepivorumsclerotiasoil451·7 daysincubatordirect platingsemiselective6% sclerAdams (1987)
S. cepivorumsclerotiasoil5019 hincubatordirect platingsemiselective6% sclerAdams (1987)
S. cepivorumsclerotiasoil503 minsteam–airdirect platingPDA2·5% sclervan Loenen et al. (2003)
Septoria lycopersicispores?43?water???Spector (1956)
Synchytrium endobioticumsporangiawater608 hwater bathstainingacid fuchsin7% sporaGlynne (1926)
Taphrina deformansmycelium?46?????Spector (1956)
Thielaviopsis basicolamyceliumagar4515 hwater bathdirect platingPDA2% resPullman et al. (1981)
T. basicolamyceliumagar501·3 minwater bathdirect platingPDA2% resPullman et al. (1981)
Verticillium albo-atrumhop vineinoculum503 hwater bathdirect platingPLY agar?Talboys (1961)
V. albo-atrumhop vineinoculum55 1 hwater bathdirect platingPLY agar?Talboys (1961)
V. albo-atrumhop vineinoculum6015 minwater bathdirect platingPLY agar?Talboys (1961)
V. albo-atrummyceliumwater53 4 minwater bathdirect platingPDA?Miller & Stoddard (1956)
V. albo-atrummicrosclerotiawater55 4 minwater bathdirect platingPDA?Miller & Stoddard (1956)
V. albo-atrummyceliumplant stem47 5 minwaterdirect platingbarley straw agar?Nelson & Wilhelm (1958)
V. albo-atrummicrosclerotiaplant stem4740 minwaterdirect platingbarley straw agar?Nelson & Wilhelm (1958)
Verticillium dahliaemyceliumagar45 8 hwater bathdirect platingPDA2% resPullman et al. (1981)
V. dahliaemyceliumagar47 2 hwater bathdirect platingPDA2% resPullman et al. (1981)
V. dahliaemicrosclerotiasoil50 3 minsteam–airdirect platingselective agar2·5% resvan Loenen et al. (2003)
Plasmodiophoromycetes
Plasmodiophora brassicaefiltered extractwater7510 minwaterbioassaycabbage?Lopez-Real & Foster (1985)
P. brassicaeroots/soilbiowaste5210 hanaerobic digesterbioassayBrassica juncea25% infRyckeboer et al. (2002a)
Oomycetes
Phytophthora cinnamomirhododendron crown/rootsinoculum40 7 daysincubatordirect platingselective agar?Hoitink et al. (1976)
Phytophthora infestansmyceliumwater45?water???Spector (1956)
P. infestanssporeswater25?water???Spector (1956)
Phytophthora ramorumwood chips/bay leavesinoculum5514 daysincubatordirect platingselective agar?Garbelotto (2003)
Pythium ultimuminfected Aloe plantswater4645 minwaterbioassayAloe variegata?Baker & Cummings (1943)
P. ultimummyceliumagar45 9 hwater bathdirect platingPDA2% resPullman et al. (1981)
P. ultimummyceliumagar5033 minwater bathdirect platingPDA2% resPullman et al. (1981)
P. ultimummyceliumsoil50 3 minsteam–airbioassaypea?van Loenen et al. (2003)
Pythium irregularerhododendron crown/rootsinoculum40 7 daysincubatorbaiting + platinglupin?Hoitink et al. (1976)
Table 5.  Temperature–time conditions for eradication of bacterial plant pathogens in compost and other systems
BacteriumInoculumFeedstock/ mediumTemp.a (°C)TimeSystemDetectionReference
MethodMediumLimitb
  • a

    Maximum, average or constant temperatures recorded.

  • b

    Detection limit estimated from experimental details for P = 0·95 as percentages of test plants infected (% inf), residue samples tested (% res), colony-forming units per g or L (cfu g−1 or cfu mL−1), or not determined or stated (?).

  • c

    Survived 50°C for 3 h using moist heat.

In compost
Erwinia amylovoracotoneaster shootsbiowaste, woodchips> 40 max 7 daysheapdilution platingM–S> 300 cfu g−1Bruns et al. (1993)
E. amylovorasuspensionbiowaste55 max56 haerated tunneldilution platingselective?Ryckeboer (2001)
Erwinia chrysanthemichrysanthemumbark60 max77 daysheapdilution platingselective8% resHoitink et al. (1976)
Pseudomonas savastanoi pv. phaseolicolabean leavesgrass, hop waste, manure35 max 4 daysheapbioassaybean?Lopez-Real & Foster (1985)
Ralstonia solanacearumpotato piecesbiowaste59 max16 haerated tunneldilution platingselective agar20 cfu mL−1 digest 1E3 cfu g−1 infected materialRyckeboer (2001)
In other systems
Clavibacter michiganensis ssp. michiganensissuspensionsewage sludge, tomato35 av 7 daysanaerobic digesterenrichment and dilution platingD2 broth & nutrient agar3E3 cfu mL−1Turner et al. (1983
E. amylovorasuspensioninoculum50 const30 minwater bathdilution platingKB?Keck et al. (1995)
E. amylovoraapple budwoodinoculum45c const 3 hincubatordilution platingKB9% infKeck et al. (1995)
Erwinia carotovora ssp. atrosepticasuspensioninoculum50 const15 minwater bathdilution platingnutrient agar?Robinson & Foster (1987)
Erwinia carotovora ssp. carotovorasuspensioninoculum50 const30 minwater bathdilution platingnutrient agar?Robinson & Foster (1987)
E. chrysanthemisuspensioninoculum50 const40 minwater bathdilution platingnutrient agar?Robinson & Foster (1987)
E. chrysanthemichrysanthemuminoculum40 const 7 daysincubatordilution platingselective10% resHoitink et al. (1976)
P. savastanoi pv. phaseolicolafiltered leaf macerateinoculum65 const10 minwater bathbioassaybean?Lopez-Real & Foster (1985)
R. solanacearumsuspensionbiowaste52 const12 hanaerobic digesterdilution platingselective agar20 cfu mL−1 digest 1E3 cfu g−1 infected materialRyckeboer et al. (2002a)
Table 6.  Temperature–time conditions for eradication of viral plant pathogens in compost and other systems
VirusInoculumFeedstock/ mediumTemp.a (°C)Time (days)SystemDetectionReference
MethodMediumLimitb
  • a

    Maximum, average or constant temperatures recorded.

  • b

    Detection limit estimated from experimental details for P = 0·95 as percentages of test plants infected or not determined or stated (?).

In compost
Cucumber greenmottle mosaiccucumber residueinoculum72 max  4heapbioassaycucumber30%Avgelis & Manios (1992)
Lettuce big vein/ Olpidiumlettuceonion waste50 const  7flasksbioassaylettuce?Coventry et al. (2002)
Melon necrotic spotmelon plantshorticultural wastes65 max 28heapbioassay/ELISAmelon?Suarez-Estrella et al. (2002)
Pepper mild mottlepepper plantshorticultural wastes65 max 70heapbioassay/ELISApepper?Suarez-Estrella et al. (2002)
Tobacco mosaictobacco leavesbiowaste74 max 48heapbioassaytobacco?Hermann et al. (1994)
Tobacco mosaictobacco leavesbiowaste31 max184vesselsbioassaytobacco?Ryckeboer et al. (2002b)
Tobacco mosaictobacco leaveshousehold, various66 av 28heapbioassay/ELISAtobacco?Christensen et al. (2001)
Tobacco mosaictobacco leavesbiowaste78 max 57aerated tunnelsbioassaytobacco?Ryckeboer (2001)
Tobacco necrosisbean leavesgrass, hop waste, manure54 ave  4heapbioassaybean?Lopez-Real & Foster (1985)
Tobacco necrosis/ Olpidiumtulip debris/soilinoculum50 av 50heapbioassaytulip15%Asjes & Blom-Barnhoorn (2002)
Tomato mosaictomato residueinoculum46 max 10heapbioassaytobacco60%Avgelis & Manios (1989)
Tomato spotted wiltpepper plantshorticultural wastes65 max  2·5heapbioassay/ELISApepper?Suarez-Estrella et al. (2002)
In other systems
Cucumber greenmottle mosaiccucumber residueinoculum72 const  3incubatorbioassaycucumber30%Avgelis & Manios (1992)
Tobacco mosaicplant juiceinoculum94 const 10 minwater bathbioassaytobacco/bean?Price (1933)
Tobacco mosaicplant juiceinoculum75 const 40water bathbioassaytobacco/bean?Price (1933)
Tobacco necrosisfiltered leaf macerateinoculum75 const 10 minwater bathbioassaybean?Lopez-Real & Foster (1985)
Tobacco rattle?inoculum75–80 const  10 minwater bath???Schmelzer (1957)
Tobacco necrosis/ Olpidiumtulip debris/soilinoculum50 av 14incubatorbioassaytulip15%Asjes & Blom-Barnhoorn (2002)
Table 7.  Temperature–time conditions for survival of viral plant pathogens in compost and other systems
VirusInoculumFeedstock/ mediumTemp.a (°C)Time (days)SystemDetectionReference
MethodMedium
  • a

    Maximum, average or constant temperatures recorded.

In compost
Cucumber green mottle mosaiccucumber residueinoculum72 max 3heapbioassaycucumberAvgelis & Manios (1992)
Tobacco rattletobacco leavesrefuse69 max 6towerbioassaytobaccoMenke & Grossmann (1971)
Pepper mild mottlepepper plantshorticultural wastes65 max56heapbioassay/ELISApepperSuarez-Estrella et al. (2002)
Tobacco mosaictobacco leavesbiowaste64 max87heapbioassaytobaccoHermann et al. (1994)
Tobacco mosaictobacco leaveshousehold, various56 av28heapbioassaytobaccoChristensen et al. (2001)
Tobacco mosaictobacco residuesbark70 max42heapbioassaytobaccoHoitink & Fahy (1986)
Tobacco mosaictobacco leavesinoculum54 max53vesselsbioassaytobaccoRyckeboer (2001)
Tobacco necrosisbean leavesgrass, hop waste, manure54 av 3heapbioassaybeanLopez-Real & Foster (1985)
In other systems
Cucumber greenmottle mosaiccucumber residueinoculum50 const30incubatorbioassaycucumberAvgelis & Manios (1992)
Cucumber green mottle mosaiccucumber residueinoculum72 const 2incubatorbioassaycucumberAvgelis & Manios (1992)
Tobacco necrosisfiltered leaf macerateinoculum65 const10 minwater bathbioassaybeanLopez-Real & Foster (1985)
Tomato mosaicseedsinoculum70 const22incubatorbioassaytobaccoBroadbent (1965)
Tomato mosaicseedsinoculum72 const22incubatorbioassaytomatoHowles (1961)
Tobacco mosaictobacco leavesbiowaste68 const12anaerobic digesterbioassaytobaccoRyckeboer et al. (2002a)
Tomato mosaictomato residueinoculum47 av70incubatorbioassaytobaccoAvgelis & Manios (1989)
Tobacco mosaicplant juiceinoculum68 const70water bathbioassaytobacco/beanPrice (1933)
Tobacco necrosis/ Olpidiumtulip debris/soilinoculum40 av35incubatorbioassaytulipAsjes & Blom-Barnhoorn (2002)
Table 8.  Temperature–time conditions for eradication of plant parasitic nematodes in compost and other systems
NematodeInoculumFeedstockTemp.a (°C)TimeSystemDetectionReference
MethodMediumLimitb
  • a

    Maximum, average or constant temperatures recorded.

  • b

    Detection limit estimated from experimental details for P = 0·95 as percentages of test plants infected (% inf), cyst surviving (% cyst), or not determined or stated (?).

In compost
Globodera rostochiensiscystspotatoes33 const?heap???Sprau (1967)
Heterodera schachtiicystsbiowaste67 max62 hvesselslarval emergenceZnCl2 soln4% cystRyckeboer (2001)
Meloidogyne chitwoodiiinfected tubers of Scorzonerabiowaste58 av42 haerated tunnelsbioassaytomato?Ryckeboer (2001)
Meloidogyne incognitapepper/tomatorefuse57 av19 hcompost silobioassaygherkin9% infMenke & Grossmann (1971)
M. incognitaegg sacsbiowaste74 max 4 daysheapbioassaypepper9% infHermann et al. (1994)
M. incognitaegg sacsbiowaste50 const30 hincubatorbioassaypepper9% infHermann et al. (1994)
In other systems
Aphelenchoides ritzemabosiinfected bulbsinoculum45 const 3 hwater bath???Becker (1974)
Globodera pallidacystssoil50 const 3 minsteam–airlarval emergencediffusate7·5% cystvan Loenen et al. (2003)
Globodera rostochiensiscystssoil60 const 3 minsteam–airlarval emergencediffusate7·5% cystvan Loenen et al. (2003)
Meloidogyne haplastrawberry rootsinoculum49 const 7 minwater bathbioassay/microscopywater30% infGoheen & McGrew (1954)
M. haplarose rootsinoculum45·5 const 1 hwater bathlarval emergencerose?Martin (1968)
M. incognitatomato rootsbiowaste52 const12 hanaerobic digesterbioassaytomato25% infRyckeboer et al. (2002a)
Meloidogyne javanicapotato tubersinoculum46 const 2 hwater bathbioassaytomato50% infMartin (1968)
M. javanicapotato tubersinoculum49 const 1 hwater bathbioassaytomato50% infMartin (1968)
Pratylenchus penetransstrawberry rootsinoculum46 const45 minwater bathmicroscopywater?Goheen & McGrew (1954)
P. penetransstrawberry rootsinoculum49 const 7·5 minwater bathmicroscopywater?Goheen & McGrew (1954)
Table 9.  Temperature–time conditions for survival of plant-parasitic nematodes in compost and other systems
NematodeInoculumFeedstockTemp.a (°C)TimeSystemDetectionReference
MethodMedium
  • a

    Maximum, average or constant temperatures recorded.

In compost
Heterodera schachtiicystsbiowaste50 max40 hheaplarval emergenceZnCl2 solnRykeboer (2001)
In other systems
Globodera pallidacystssludge35 av10 daysanaerobic digesterlarval emergencediffusateTurner et al. (1983)
Heterodera schachtiicystsbiowaste52 const30 minanaerobic digesterlarval emergenceZnCl2 solnRyckeboer et al. (2002a)
Meloidogyne javanicapotato tubersinoculum47·5 const1 hwater bathbioassaytomatoMartin (1968)
Meloidogyne haplarose rootsinoculum44·5 const2 hwater bathlarval emergenceroseMartin (1968)
M. haplarose rootsinoculum45·5 const30 minwater bathlarval emergenceroseMartin (1968)
M. haplastrawberry rootsinoculum44 const1 hwater bathmicroscopywaterGoheen & 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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Systems used for studying temperature–time effects on eradication
  5. Methods used for assessing survival of plant pathogens and nematodes during composting
  6. Temperature–time effects on plant pathogens and nematodes
  7. Other compost factors involved in pathogen eradication
  8. Temperature profiling of commercial composting systems
  9. Conclusions
  10. Acknowledgements
  11. References

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

Bioassays

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).

Plating

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.

Serological methods

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

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

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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Systems used for studying temperature–time effects on eradication
  5. Methods used for assessing survival of plant pathogens and nematodes during composting
  6. Temperature–time effects on plant pathogens and nematodes
  7. Other compost factors involved in pathogen eradication
  8. Temperature profiling of commercial composting systems
  9. Conclusions
  10. Acknowledgements
  11. References

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)

Fungi

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).

Oomycetes

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).

Plasmodiophoromycetes

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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Systems used for studying temperature–time effects on eradication
  5. Methods used for assessing survival of plant pathogens and nematodes during composting
  6. Temperature–time effects on plant pathogens and nematodes
  7. Other compost factors involved in pathogen eradication
  8. Temperature profiling of commercial composting systems
  9. Conclusions
  10. Acknowledgements
  11. References

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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Systems used for studying temperature–time effects on eradication
  5. Methods used for assessing survival of plant pathogens and nematodes during composting
  6. Temperature–time effects on plant pathogens and nematodes
  7. Other compost factors involved in pathogen eradication
  8. Temperature profiling of commercial composting systems
  9. Conclusions
  10. Acknowledgements
  11. References

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.

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Systems used for studying temperature–time effects on eradication
  5. Methods used for assessing survival of plant pathogens and nematodes during composting
  6. Temperature–time effects on plant pathogens and nematodes
  7. Other compost factors involved in pathogen eradication
  8. Temperature profiling of commercial composting systems
  9. Conclusions
  10. Acknowledgements
  11. References
  • • 
    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.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Systems used for studying temperature–time effects on eradication
  5. Methods used for assessing survival of plant pathogens and nematodes during composting
  6. Temperature–time effects on plant pathogens and nematodes
  7. Other compost factors involved in pathogen eradication
  8. Temperature profiling of commercial composting systems
  9. Conclusions
  10. Acknowledgements
  11. References

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.

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  1. Top of page
  2. Abstract
  3. Introduction
  4. Systems used for studying temperature–time effects on eradication
  5. Methods used for assessing survival of plant pathogens and nematodes during composting
  6. Temperature–time effects on plant pathogens and nematodes
  7. Other compost factors involved in pathogen eradication
  8. Temperature profiling of commercial composting systems
  9. Conclusions
  10. Acknowledgements
  11. References
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