Irrig Sci (2011) 29:267–297

DOI 10.1007/s00271-011-0285-1

REVIEW

Plant pathogens in recycled irrigation water in commercial plant nurseries and greenhouses: their detection and management

Sally M. Stewart-Wade

Received: 1 February 2011 / Accepted: 4 April 2011 / Published online: 23 April 2011© Springer-Verlag 2011

Abstract With water conservation and reuse a priority forcommunities worldwide, recycling irrigation water in com-mercial plant nurseries and greenhouses is a logical mea-sure. Plant pathogenic microorganisms may be present inthe initial water source, or may accrue and disperse fromvarious points throughout the irrigation system, constitutinga risk of disease to irrigated plants. The continual recyclingof this water is exacerbating this plant disease risk. Accu-rate and timely detection of plant pathogenic propagules inrecycled irrigation water is required to assess disease risk.Both biological and economic thresholds must be estab-lished for important plant-pathosystems. Plant pathogens inrecycled irrigation water can be managed by a variety oftreatment methods that can be arranged in four broad cate-gories: cultural, physical, chemical, and biological. An inte-grated approach using one or more techniques from eachcategory is likely to be the most eVective strategy in com-bating plant pathogens in recycled irrigation water.

Introduction

Water used for irrigation in commercial plant nurseries andgreenhouses can be captured for reuse. Initial irrigationwater can be sourced from surface water supplies such asponds, lakes, rivers, and reservoirs. However, these can har-bor disease-causing microorganisms, with almost everymajor group of plant pathogens having been found in such

sources (Hong and Moorman 2005). In addition to this con-tamination of the initial source, plant pathogens may get intothe water at various points of the irrigation regime, espe-cially if the water comes into contact with plant debris orsoil (Hong and Moorman 2005). Due to the numerous envi-ronmental and ecological advantages to recycling irrigationwater (Schnitzler 2004), there is a strong push to recycleirrigation water for agricultural and horticultural purposes(Norman et al. 2003; NGIA 2005). With water becomingmore costly and harder to access in many countries through-out the world, and with its recognition as a valuable, Wnitecommodity, the international community is calling for moreresponsible use of water resources (Rolfe et al. 2000). How-ever, with the increased use of recycled water for irrigationin commercial plant nurseries and greenhouses comes a con-comitant increase in the potential dispersal of plant patho-gens and so, an elevated disease risk.

Recycled irrigation water acts as both a primary inocu-lum source and an eVective inoculum dispersal mechanismin many plant-pathosystems, correlating to plant disease(Faulkner and Bolander 1970; Grech and Rijkenberg 1992;Klotz et al. 1959; Lacy et al. 1981; Van Kuik 1992; White-side and Oswalt 1973; Hong et al. 2001; Bewley andBuddin 1921). Infected plants may harbor and liberate largenumbers of infective propagules of pathogens into leachatewater, which are then delivered to the holding pond and,when the water is recycled for irrigation, are subsequentlyredistributed to susceptible crops (MacDonald et al. 1994).Plants irrigated with water containing plant pathogens canresult in plants displaying disease symptoms and plantdeath, and therefore an increase in unsaleable plants;increased use of pesticides to control disease outbreaks(which means increased production costs); and diseasespread to previously uninfected production areas (Jameset al. 1995a).

Communicated by J. Ayars.

S. M. Stewart-Wade (&)Melbourne School of Land and Environment, The University of Melbourne, Burnley Campus, 500 Yarra Blvd, Richmond, VIC 3121, Australiae-mail: smsw@unimelb.edu.au

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Various production methods can inXuence disease, suchas irrigation method and timing. For instance, an ebb andXood irrigation system appears to reduce disease incidencecompared to an overhead irrigation system (Hoitink et al.1992). However, important nursery diseases, such as thosecaused by Pythium spp. can still be transmitted by thismethod (Hoitink et al. 1992; Sanogo and Moorman 1993).Therefore, such practices need to be evaluated for their con-tributory eVect on plant disease within the production system.

A survey conducted in 2000–2002 on the recycling ofnutrient solutions in the greenhouse industry in Ontario,Canada found that 33% of growers who use recirculatingsystems cite disease control as a major problem, and thatthis area required more research (Richard et al. 2006). Sim-ilarly, an Australian study by Lane (2004) identiWedresearch on treating recycled irrigation water to controlplant pathogens as a high priority for the nursery industry.With the public demanding and governments legislating forthe responsible use and reuse of water resources, the issuesof increased disease risk and practical management strate-gies are becoming increasingly important. Hong and Moor-man (2005) reviewed this topic, but since their publication,more disinfestation and treatment systems have been devel-oped, which warrant examination.

Types of plant pathogens in recycled irrigation water

Fungi and fungal-like organisms

Many fungi and fungal-like organisms have been found inrunoV water, and while some have been implicated in caus-ing disease in various crops, for others, their signiWcancehas not been determined (Hong and Moorman 2005; Honget al. 2002a, c; Hong and Epelman 2001). MacDonald et al.(1997) demonstrated that the use of recycled irrigationwater containing plant pathogens presented a signiWcantdisease risk with prolonged irrigation.

Some of the more important plant pathogenic fungi andfungal-like organisms detected in recycled irrigation wateror recirculating nutrient solutions of hydroponic systems(Hong and Moorman 2005) include: Phytophthora, Pyth-ium, Olpidium brassicae (vector for several damagingviruses), Alternaria, Botrytis, Rhizoctonia (Anonymous2007; Hong and Moorman 2005), Fusarium oxysporum,Colletotrichum coccodes, Phomopsis sclerotioides, Thiel-aviopsis basicola (sexual state of Chalara elegans), Verti-cillium (Jenkins and Averre 1983; McPherson et al. 1995),Cylindrocladium (MaWa et al. 2008), Sclerotinia sclerotio-rum (Steadman et al. 1974), Gnomonia radicicola (Amsing1995), and Sclerotium (Shokes and McCarter 1978).

Source water and recycled irrigation water have beendocumented repeatedly as being responsible for the intro-

duction and spread of pythiaceous species such as membersof Phytophthora and Pythium, which possess swimmingzoospores, in Weld, orchard and greenhouse crops (Gill1970; Klotz et al. 1959; McIntosh 1966; Pittis and Colhoun1984; Shokes and McCarter 1979; Thomson and Allen1974; Whiteside and Oswalt 1973; Menzies et al. 1996;Bush et al. 2003; Pettitt et al. 1998; Werres et al. 2007).

Seasonal variation in the inoculum load and speciesdiversity in irrigation water have been reported (Thomsonand Allen 1974), and therefore inXuences the treatment ofsuch water applied to nursery crops (Ali-Shtayeh et al.1991). MacDonald et al. (1994) found that the number ofpropagules of Phytophthora and Pythium species recoveredfrom water in eZuent holding ponds in three Californiannurseries, varied greatly from month to month in numberand species diversity, and Pythium propagules were consis-tently the most numerous recovered. However, informationis generally scant on the inoculum load and species diver-sity in recirculated nursery water in many other parts of theworld (Anonymous 2007). This information is required tothen assess the eYcacy of disinfestation treatments againstrealistic concentrations of propagules.

Bacteria

Various plant pathogenic bacteria can be present in waterused for irrigation and cause disease on crops (Hong andMoorman 2005). Erwinia species, that cause soft rots ofpotatoes and ornamental species, have been recorded insurface water used for irrigation in USA and Scotland(Harrison et al. 1987; McCarter-Zorner et al. 1984; Cappaertet al. 1988; Gudmestad and Secor 1983; Lacy et al. 1981;Norman et al. 2003). Pseudomonas solanacearum (Jenkinsand Averre 1983) and Clavibacter michiganensis (vonGriesbach and Lattauschke 1991) were reported as beingdisseminated in the nutrient solutions of hydroponic sys-tems. Xanthomonas campestris pv. begoniae was able tospread in a recycled ebb-and-Xow irrigation system for theproduction of begonias in the USA, causing low levels ofdisease (Atmatjidou 1991).

Viruses

Several viruses have been detected in irrigation systemsusing recycled water (Hong and Moorman 2005) and inrecirculated nutrient solutions (Berkelmann et al. 1995;Paludan 1985; Pares et al. 1992; Büttner 1995; Rosner et al.2006). Arabis mosaic virus (ArMV), cucumber greenmosaic virus (CGMV), cucumber mosaic virus (CMV), let-tuce big vein agent (LBVA), melon necrotic spot virus(MNSV), pelargonium Xower break virus (PFBV), pelargo-nium leaf curl virus (PLCV), tobacco mosaic virus (TMV),tobacco necrosis virus (TNV), tomato mosaic virus

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(ToMV), and tomato spotted wilt virus (TSWV) werespread in recirculating nutrient solutions in soilless cultures(Paludan 1985; Tomlinson and Faithfull 1980; Tomlinsonand Thomas 1986; Büttner 1995; Berkelmann et al. 1995).Virions of ToMV were detected in the nutrient solution3 days after leaf inoculation of plants and these virionsremained infective for at least 6 months (Pares et al. 1992).

Nematodes

Plant parasitic nematode genera have been found in irriga-tion water (Hong and Moorman 2005; Faulkner andBolander 1970; Amsing and Runia 1995; Steadman et al.1974). However, the survival and infectivity of at leastsome species seems to be curtailed by using overhead irri-gation systems, where it has been speculated that the pres-sure at the pump or in the sprinkler nozzles is detrimental tothe nematode larvae (Heald and Johnson 1969).

Detecting plant pathogens in recycled irrigation water

To determine whether a pathogen is present in irrigationwater, it is important to ascertain both the detection thresh-old (if the pathogen can be detected using particular sam-pling methods) and the biological threshold (to measure theinoculum level and its frequency to ascertain its diseasepotential) (Hong and Moorman 2005). This will aid indetermining the economic injury level (Steinberg et al.1994; Ehret et al. 2001) and therefore whether the expenseof a disinfestation program is justiWed.

Detection threshold

The detection threshold of the sampling and quantiWca-tion method is important to determine the number, vol-ume, location, and timing of collection of the samplesrequired (Hong and Moorman 2005). These variables aredetermined through trial and error using test samplesspiked with known quantities of propagules of the patho-gen of interest (Hong and Moorman 2005). The temporalXuctuation in both the size and species composition ofthe microbial population in water has been well docu-mented (Shokes and McCarter 1979; Themann et al.2002a, b; Thomson and Allen 1974; Werres et al. 2007;Bush et al. 2003; Faulkner and Bolander 1970; Harrisonet al. 1987; Thinggaard and Middelboe 1989; Hong andMoorman 2005; MacDonald et al. 1994). The spatialdistribution, both vertically and horizontally, has beenreported to Xuctuate for some populations in water(Shokes and McCarter 1979; Bush et al. 2003; Wilsonet al. 1998; Hong and Moorman 2005; Rattink 1990)Awareness of the potential for temporal and spatial

Xuctuations will determine the optimal parameters forsampling.

Filters and selective plating

Filters or sieves can be used to retain plant pathogens,allowing quantitative evaluations, and so enabling calcula-tions of disease threshold levels in irrigation water (Honget al. 2002b; Bush et al. 2003). The Wlters can then beplaced directly onto an appropriate growth medium, or theWltrand can be washed from the Wlter and spread onto thegrowth medium (Hong and Moorman 2005). In a study onisolating pythiaceous species from various sources of irri-gation water, Hong et al. (2002b) found that directly invert-ing Wlters onto isolation media produced more consistentresults than spreading the washed Wltrand and was simplerand quicker; however, colonies were more diYcult to quan-tify and purify since they were in such close proximity tothe membrane on the plate.

The sensitivity of Wlter-based detection is vital in theaccurate assessment of the disease potential of plant patho-gens in recycled irrigation water. For instance, Pythiumaphanidermatum spread from plants growing in infestedmedia to plants growing in noninfested media in an ebb-and-Xow subirrigation system, yet the pathogen was notdetected in the irrigation water using Wlter-based isolation(Sanogo and Moorman 1993). The eYcacy of diVerentmembranes to detect pythiaceous species in various irriga-tion water sources was tested (Hong et al. 2002b). Themembranes diVered mainly in their pore size and theirmaterial composition (Hong et al. 2002b). A Wlter with arelatively large pore size (5 �m) showed greater recoveryrates of pythiaceous species than other Wlters from variouswater sources. In addition to its superior sensitivity, Wlter-ing time was reduced (Hong et al. 2002b). It is also impor-tant to use a standard sample volume, since diVerent samplevolumes can result in diVerent propagule concentrationestimates (McCracken and JeVers 2000).

Baiting

Selected plant parts or whole (trap) plants can bait plantpathogens from irrigation water and the colonized tissuecan be plated onto a suitable, semi-selective growthmedium (Hong and Moorman 2005; Bush et al. 2003). Thisis a sensitive method, but only provides qualitative data(Hong et al. 2002b). Shokes and McCarter (1979) foundthat Pythium spp. were recovered by baiting even whenthey were undetectable when directly plated onto selectivemedia. This is probably due to zoospores being activelyattracted to suitable baits and being able to germinate andgrow somewhat protected in the bait tissue (Bush et al.2003). When attempting to isolate various Phytophthora

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species from recycled irrigation water, baiting was moresuccessful in recovering isolates for species identiWcationthan were Wltration methods (Steddom 2009).

When baiting for plant pathogens, the location of the baitis very important. When baiting for Phytophthora in recy-cled irrigation water at a container nursery in Virginia,USA, Bush et al. (2002) found only two species of Phy-tophthora were recovered from baits placed on the surfaceof the irrigation reservoir, while a greater diversity of spe-cies were recovered from baits placed at depths (Bush et al.2003). Ghimire et al. (2006) found, during the wintermonths, Phytophthora recovery was generally greatest atthe surface compared to depths of 0.5, 1, 1.5, and >1.5 m.Yet in a later study, Ghimire et al. (2009) found Phytoph-thora recovery was greatest at the bottom of the irrigationrunoV containment basin across all months (Nov., Jan.,Mar., Aug.), while recovery from the surface and 0.5 m wasvariable in diVerent baiting months.

Exposure duration of the bait and recovery medium arealso important parameters. In studies baiting for Phytoph-thora spp. in irrigation runoV containment basins, the numberof infected baits and the diversity of species increased withincreasing exposure duration (Hong et al. 2003a; Ghimireet al. 2009). Hong et al. (2003a) compared exposure dura-tions of 1, 2, 4, 8, 24, and 48 h and found the percentage ofinfected baits increased to 24 h, when there was no diVerencebetween 24 and 48 h. Ghimire et al. (2009) tested muchlonger exposure durations, comparing 2, 7, and 14 days andfound 7 days to be optimal for recovering Phytophthora, withbaiting for 14 days increasing Pythium colonization andreducing Phytophthora colonization. The authors also foundthat there was no signiWcant diVerence in recovery of Phy-tophthora species between two recovery media, PARPH-V8and PARP-V8 (Hong et al. 2003a; Ghimire et al. 2009),although Hong et al. (2003a) recommended using PARPH-V8, which contains hymexazole, a compound that limits thegrowth of faster growing Pythium spp.

The choice of bait species is obviously important, butalso the bait type, whether whole leaves or leaf disks, caninXuence recovery of pathogens of interest. When baitingfor Phytophthora, whole rhododendron leaves were the bestbaiting material among six bait plant species and type com-binations assessed, including camellia and holly (Ghimireet al. 2009). Wilson et al. (1998) found lemon leaf baitswere equally eVective as rhododendron in recovering Phy-tophthora spp.. Irrespective of bait plant species, whole leafbaits gave greater recovery of Phytophthora species thanleaf disks (Ghimire et al. 2009).

Immunochemical methods

Immunochemical techniques can facilitate the rapid detec-tion of low numbers of pathogen propagules (Hong and

Moorman 2005), and to date, have been used for detectingPhytophthora and Pythium. Commercial ELISA kits wereuseful in detecting both Pythium and Phytophthora in watersamples, though diVerentiation of the two genera was notpossible (Ali-Shtayeh et al. 1991). Also, a membrane Wltra-tion assay using polyclonal antisera has been developed forthe detection of Pythium zoospores in irrigation water(Wakeham et al. 1997). Zoospore suspensions were Wlteredthrough nitrocellulose membranes and germinating zoo-spores were probed with polyclonal antibodies. The assaypositively identiWed all Pythium spp. tested, as well as zoo-spores of Phytophthora cryptogea.

Two serological detection assays, namely the zoosporetrapping immunoassay and the dipstick assay, were com-pared with two conventional assays, namely Wltration withselective plating and baiting, for their sensitivity in detect-ing propagules of two species of Pythium and two speciesof Phytophthora (Pettitt et al. 2002). In initial comparisonswith propagules in dilution series in sterile water, the zoo-spore trapping immunoassay was the most sensitive assayfor all four species, followed by the Wltration with selectiveplating assay, and the dipstick and baiting assays were con-siderably less sensitive (Pettitt et al. 2002). When compar-ing their detection eYcacy with water samples fromhorticultural nurseries, the zoospore trapping immunoassaywas again the most sensitive, though the Wltration withselective plating assay gave more consistent results (Pettittet al. 2002). In a similar study, an ELISA assay was com-pared to direct plating and three baiting tests, namely apple,lupin, and rhododendron (Themann et al. 2002a). The rho-dodendron test trapped the widest range of Phytophthoraspecies and was the most successful method, followed bythe ELISA test with antiserum against P. cinnamomi(Themann et al. 2002a).

Molecular methods

Molecular methods, such as polymerase chain reaction(PCR) ampliWcation of DNA, can be used to detect plantpathogens from water (Hong and Moorman 2005). DNAcan be extracted from Wltrands, colonies on media or baitsand then ampliWed using universal or species-speciWc prim-ers (Kong et al. 2003a, b; Hong and Moorman 2005). PCRproducts can subsequently be analyzed for particular band-ing patterns using gel electrophoresis, probed with species-speciWc fragments, or sequenced and identiWed using genedatabases (Hong and Moorman 2005). PCR assays such asthese can be more rapid, speciWc, and sensitive than tradi-tional detection techniques, but problems can arise sinceirrigation water contains a variety of microbes, pesticideresidues, and organic contamination that may cause crossreactions or inhibition of reactions (Kong et al. 2003a).PCR assays reduce detection time from at least a week for

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traditional Wlter/bait/plating methods, to a few hours. Tradi-tional techniques are more tedious, requiring signiWcantexpertise to diVerentiate species of pathogens, while PCRassays are easy to use and require minimal training (Konget al. 2003a). Also, serological methods such as ELISA canyield false positive results for closely related genera(Ali-Shtayeh et al. 1991), whereas PCR assays can behighly speciWc (Kong et al. 2003a). Finally PCR assays canbe more sensitive at detecting low levels of pathogens(Kong et al. 2003a), whereas the detection threshold usingtraditional methods may be above the biological thresholdfor particular pathogens (Hong et al. 2002b; Hong andEpelman 2001).

Detection issues

It is important to determine the resolution and accuracy ofdetection methods to avoid false negatives, i.e., not Wndingthe plant pathogen of interest that is present in the water, asmuch as possible (Hong and Moorman 2005). To facilitatethis, molecular methods should always include positive andnegative controls (Hong and Moorman 2005).

Biological threshold

Biological thresholds will be diVerent for diVerent host-pathosystems. There has been limited study on the biologi-cal threshold of individual plant pathogens in irrigationwater (Hong and Moorman 2005), and no research on theinteractions among and between pathogens and othermicrobes (Hong and Moorman 2005). The occurrence ofeven low concentrations of plant pathogenic propagulesmay represent a disease threat to susceptible hosts due tothe luxurious volumes of water applied to nursery stock(Smith et al. 1985) and repeated inoculation with each irri-gation event.

Inoculum level versus inoculum potential

The amount of inoculum required to cause disease dependson the frequency of the exposure to the pathogen (Hong andEpelman 2001), the irrigation method (Stanghellini et al.2000), and the soil or growing media (Hong and Moorman2005; Boehm and Hoitink 1992; Spencer and Benson1982). Determination of the biological threshold for indi-vidual plant pathogens is important since while somepathogens may be highly virulent with a high inoculumpotential, other pathogens may have an innate low inocu-lum potential, but repeated application of low levels ofthese pathogens may increase their inoculum potential(Hong and Moorman 2005; Hong and Epelman 2001).

Hong et al. (2001) found 10 species of Phytophthora inrecycled irrigation water, all at levels suYcient to cause

disease on susceptible plants (Hong and Epelman 2001).However, while no general biological threshold has beenestablished for Phytophthora spp. (Lutz and Menge 1991;Themann et al. 2002b; Reeser 1998), a concentration as lowas 18 zoospores/mL of Phytophthora cinnamomi and <74zoospores/mL of Phytophthora ramorum in recycled irriga-tion water was suYcient to cause high levels of disease insusceptible plants (Van Kuik 1994; Werres et al. 2007).Similarly, a biological threshold for Pythium spp. has notbeen determined accurately, but high inoculum levels(2 £ 106 cfu/100 L of nutrient solution) of P. aphanider-matum caused all cucumber plants to die 7–28 days afterinoculation, while low inoculum levels (2 £ 103, 22, 2.2,and 0.22 cfu/100 L of nutrient solution) reduced the growthand yield of plants in recirculating hydroponic culture ofcucumbers (Menzies et al. 1996). These yield losses maynot be obvious to growers but economically could accumu-late to be a substantial loss.

Economic threshold

There are no accurate, scientiWcally derived economicthresholds for plant pathogens in recycled irrigation water(Wilson et al. 1998).

Managing disease caused by plant pathogens in recycled water

There are many issues to consider when assessing theeYcacy of disinfestation treatment methods. For instance,the life cycle stage of the pathogen (i.e., the type of propa-gule present) can be important, with fungal spores that arethick-walled (e.g., chlamydospores) being more resistant totreatments such as UV and chlorine dioxide, than thin-walled propagules (e.g., zoospores or mycelia) (Mebaldset al. 1997b). Also, consideration should be given as to theeVect of complete disinfestation on natural disease suppres-siveness and plant- and microbial-derived metabolites;whether managing pathogens (especially with 100%eYcacy) is economically justiWed; and grower acceptanceof a tolerance threshold (Steinberg et al. 1994; van Os andAlsanius 2004; van Os 2000; Ehret et al. 2001). Impor-tantly, care must be taken with all disinfestation proceduresto avoid recontamination with pathogens that would nullifythe treatment (Rey et al. 2001), via good hygiene and regu-lar monitoring.

Several factors inXuence the amount of used irrigationwater that is collected to be recycled, and potentially thesupply water that needs to be disinfested (van Os 2000).These include the season; the timing and number of irriga-tions per day; and the type and age of crop; among others.Disinfestation of smaller volumes, such as those used in

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hydroponic systems, is feasible, but large volumes at highpumping rates such as in large nursery production systems,may become uneconomic to disinfest (van Os 2000;MacDonald et al. 1994).

This section is divided, somewhat artiWcially in someinstances, into cultural, physical, chemical, and biologicalmethods for the management of plant pathogens in recycledwater.

Cultural

Avoidance

It is important to prevent plant pathogens from being intro-duced into water sources, e.g., holding ponds, by prevent-ing contaminated soil and plant debris from being carriedinto the water (Hong and Moorman 2005). Also, irrigationintake pipes should be positioned at depths or locations toavoid uptake of pathogenic propagules (Armitage 1993;Hong and Moorman 2005; Rattink 1990; Bush et al. 2003;Shokes and McCarter 1979; Themann et al. 2002a, b;Wilson et al. 1998). For example, Hong et al. (2003b)found that the recovery of Phytophthora spp. decreasedwith increasing distance from the runoV entrance into aholding pond, implying that the location of the pump houseto recycle such water can be important for avoiding highlevels of inoculum. Similarly, Rattink (1990) and Wilsonet al. (1998) found plant pathogenic propagules in still orslow moving water generally settled to the base of retentionbasins and holding containers where they began to degrade.The intake pipe for pumping the solution was located awayfrom the base, therefore no or few propagules were trans-ported (Rattink 1990). In addition, recycled irrigation watercould be stored for a period of time to allow for the viabilityof short-lived pathogenic inoculum to expire (Van Kuik1992). For example, zoospores of P. cinnamomi were non-viable after 35 h at 20°C or 46 h at 15°C, so storing col-lected irrigation water for such periods at certaintemperatures could decrease or remove inoculum of certainspecies prior to recycling onto production areas (Van Kuik1992).

Inoculum reduction

Irrigation type, duration, and timing can aVect the produc-tion of pathogenic inoculum and resultant plant disease inrecycled irrigation water (Nielsen et al. 2004; Hong andMoorman 2005). Pulse irrigation (trickle or drip irrigationadding only measured amounts of water required by theplants) minimizes excess water, and consequently, runoV(containing propagules from the crop and contaminatedsoil) can be reduced by up to 77% (Kabashima 1993; Hongand Moorman 2005). Similarly, with two, 30-min daily

irrigations, disease onset due to Phytophthora occurred2 weeks earlier and spread throughout the irrigation systemthree times faster than with two, 5 min daily irrigations.Also, with night-time irrigations, disease onset occurred3 weeks earlier and spread seven times faster than with day-time irrigations. Similarly, ebb-and-Xow benches can beless conducive to pathogen spread than top-irrigated sys-tems (Stanghellini et al. 2000). In an ebb-and-Xow system,lowering the watering frequency inhibited the incidence ofdisease on gerbera caused by P. cryptogea (Thinggaard andAndersen 1995). Also, raising the soluble salt concentration(electrical conductivity) of the solution, either alone or incombination with reduced watering frequency, reduced thedisease incidence (Thinggaard and Andersen 1995).

Physical

Barriers

Physical barriers such as mats and Wlms can inhibit thespread of pathogenic propagules. In an ebb-and-Xow irriga-tion system, the use of an irrigation mat signiWcantlyreduced the spread of Phytophthora rot in gerbera wheninoculum had been applied to pots, or zoospores wereapplied to irrigation tanks. Irrigation mats, consisting of athin layer of polyethylene on the base with a thicker layerof polypropylene and acryl on top, appeared to act as a bar-rier to the movement of inoculum out of or into the pot (vander Gaag et al. 2001).

Sedimentation

Electro-coagulation produces positive and negative ions viaan electric current that then attract negatively and positivelycharged contaminants in recycled irrigation water, respec-tively, such as bacteria, viruses, nematode cysts, as well aspesticides, organic species, metals, and suspended solids.The resulting reaction products coagulate and precipitateout of solution, forming a sludge (Chin 2005). This methodis simple, safe, and easy to use, inexpensive to run and isnot aVected by variations in the water (Chin 2005). It is,however, expensive to install and the sludge need to beremoved regularly (Chin 2005).

Filtration

Filtration of recycled irrigation water can be achieved bytwo main methods: slow media or membrane Wlters. Forbiological Wltration, see the Section “Biological”.

Slow media Slow media Wltration involves passing waterthrough a Wlter medium at a slow rate to remove undesir-able microorganisms such as fungi, fungal-like organisms,

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bacteria, nematodes, and viruses (Wohanka 1995). It alsoimproves the quality of the water by removing suspendedparticulates (Barth 1998). Sand is the most commonly usedmedium but other media in use or under investigationinclude rockwool (stonewool), pumice (lava grains), acti-vated charcoal, silica, vermiculite, perlite, porous clay (Ser-amis®), and anthracite (Wohanka et al. 1999; Park et al.1998). This method removes pathogens while retaining partof the natural microXora, and as such, preserving the innatedisease suppressiveness present in recycled irrigation water(Déniel et al. 2004; Postma et al. 2000; van Os and Postma2000).

The eYcacy of slow Wltration is due to the complexinteraction of mechanical, physico-chemical, and biologicalfactors (Brand and Wohanka 2001; Weber-Shirk and Dick1997a, b) [so slow Wltration cannot be classed exclusivelyas a physical method and inclusion in this section, asopposed to the section on biological methods, is somewhatarbitrary]. The mechanism of action of slow Wltration is notfully understood but it is proposed that Wlters act as a phys-ical sieve, but also house a diverse population of microbesthat actively interact with microorganisms in the recycledwater (Brand and Wohanka 2001; Calvo-Bado et al. 2003b;Weber-Shirk and Dick 1997a, b). Mechanical and physico-chemical factors aVect the eYcacy of the Wlter against fun-gal and bacterial plant pathogens, with low Xow rates and aWlter medium with a large surface area and small pores gen-erally improving the eYcacy (Furtner et al. 2007). Steviket al. (2004) reviewed the factors that determine the reten-tion of bacterial pathogens in slow Wltration systems andfound the main mechanisms were straining and adsorption,inXuenced by the Wlter media (including porosity and grainsize) and its organic content, characteristics of the pathogen(including size, shape, concentration, hydrophobicity, bio-Wlm production), Xow rate, temperature, pH and ionicstrength, and species (Furtner et al. 2007).

Factors aVecting biological activity, such as low temper-ature and oxygen deWciency, interfere with Wlter eYcacyand so demonstrate the importance of the biological com-ponent of slow Wltration (Brand and Alsanius 2004a; Ellis1985; Van Kuik 1994). It is further indicated by the lowereYcacy of both steam sterilized Wlters (Brand andWohanka 2001) and “fresh” or “unripened” Wlters (Mineet al. 2003) compared to “biologically ripened” Wlters(Furtner et al. 2007), though the composition and impor-tance of the microbial Xora against individual pathogens isnot well characterized (Brand and Wohanka 2001). EYcacycan be improved by expediting the biological activation ofthe Wlter via inoculation of the media with selected bacterialstrains (Déniel et al. 2004). Three strains of Pseudomonasputida had a plant growth promoting eVect, and two strainsof Bacillus cereus had an antagonistic eVect (Déniel et al.2004). However, the importance of the biological compo-

nent seems to be dependent on the pathogen species. Dénielet al. (2004) showed that elimination of Pythium spp. byslow Wltration appears to rely mainly on physical factors,since both biologically activated and non-biologically acti-vated Wlters showed a high eYcacy for eliminating Pythiumspp. from the Wrst month onwards. Similarly, van Os et al.(1999) showed there was no diVerence in the elimination ofP. cinnamomi between mature and immature Wlters, orbetween Wlters with a high or low biological load, indicat-ing that physical factors, including the attachment betweenpathogenic propagules and sand grains, were more impor-tant than biological factors. Conversely, elimination ofF. oxysporum by slow Wltration appears to be more inXu-enced by biological factors, since the non-biologically acti-vated Wlter only reached its best eYcacy after 6 months,while the biologically activated Wlter showed a higheYcacy from the Wrst month onwards (Déniel et al. 2004).

Further work on biological enhancement of the Wlter hasincluded the addition of a fungal cell wall preparation toenhance its cell wall-degrading enzyme activity (Furtneret al. 2007). Brand and Alsanius (2004a) found indicationsof improved Wlter eYcacy against F. oxysporum f. sp.cyclaminis with induction of enzyme activity due to theaddition of the lyophilized pathogen to the “schmutzdecke”(surface biological mat), but the work of Furtner et al.(2007) did not support this Wnding. Cell wall-degradingenzymes also naturally occurred in such systems, with thehighest protease activity in the schmutzdecke (Brand andAlsanius 2004b).

Most authors agree that slow Wltration is a reliable,eVective, and relatively inexpensive method for disinfest-ing recycled irrigation water (Brand and Alsanius 2004a;Van Kuik 1994; van Os et al. 1998; Weber-Shirk andDick 1997b; Calvo-Bado et al. 2003b). The cost of estab-lishing a slow Wltration system depends on the size andcomposition of the holding tanks required, and the avail-ability and suitability of locally available sand or alterna-tive media (Barth 1998). Other advantages include thatthere are low maintenance requirements; no issues withpH as for some other treatment methods; no harmfulresiduals remain in the treated water; no chemicals areused enhancing user safety; no technical instrumentation;it is a low energy consuming process; it is adaptable to awide range of production systems; and the technology isrobust and relatively simple from a grower’s perspective,able to be built from basic components and installed bylaymen (Chin 2005; Barth 1998, 1999). Also, retention ofpart of the natural microXora may increase disease sup-pressiveness, and this may mean that complete elimina-tion of disease-causing propagules may not be necessary(Barth 1998; Déniel et al. 2004; Postma et al. 2000; vanOs and Postma 2000). Reducing propagule numbers tolow levels, below the biological threshold where the

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chance of reinfection of a crop is negligible, may beacceptable (Barth 1998).

However, Tu and Harwood (2005) report that slow Wltra-tion has many disadvantages, including requiring largeinfrastructure; it is too slow to deliver large scale quantitiesof recycled water; the desired Wltration level is diYcult toachieve due to non-uniform porosity (which can be some-what overcome by media choice); the quality of the Wltrateis limited by particle size of the medium and the degree ofcompaction; and sediment clogging requires frequent main-tenance. In addition, Legionella bacteria (including poten-tial human pathogens) have been detected as a dominantpart of the total bacterial population in slow sand Wlters andso care is required when handling or replacing Wlter sand(Calvo-Bado et al. 2003a). Also, it is not recommended tohouse slow sand Wlters within glasshouses, due to increasedtemperatures increasing the populations of Legionella(Calvo-Bado et al. 2003a). The authors suggest regularmonitoring and disinfection, in conjunction with operatingprocedures to minimize any hazard to nursery personnel(Calvo-Bado et al. 2003a). Finally, eYcacy breakdownsoccasionally occur often with propagule removal ratesdropping from 100% to 80–90% and are apparently linkedto high levels of EC in the water (Pettitt 2002).

Sand When sand is used as the Wlter medium in slowWltration, it is often termed slow sand Wltration (SSF). SSFhas been used for more than 100 years for the treatment ofmunicipal water sources and employed for the removal ofplant pathogens from recycled irrigation water for the pasttwo decades (Wohanka 1995; Wohanka et al. 1999). InEurope, SSF has been adopted widely by the greenhousecrop production and nursery industries (Barth 1998).

Propagules of a number of plant pathogens have beeneliminated from recycled irrigation water using SSF sys-tems, including Fusarium, Phytophthora, Pythium, Cylind-rocladium, Thielaviopsis, Verticillium, the bacterial genusXanthomonas, and the nematode Radopholus similis (Ng1999; Calvo-Bado et al. 2003b; van Os et al. 1999; Brandand Wohanka 2001). Viruses, such as PFBV and ToMV,could not be removed, but for PFBV, passing the contami-nated nutrient solution through an SSF system reduced thevirus titer, caused a delay in the infection of the plants of6 weeks, and reduced disease incidence by 75% (Krczalet al. 1995; Berkelmann et al. 1995).

EYcacy of SSF is not only pathogen dependent, but italso aVected by the grade of the sand used in the Wlter. Ingeneral, the Wnest sands (0.15–0.35 mm) are more eYcientthan medium/coarse (0.5–1.6 mm) fractions of the Wne sandgrade for the control of plant pathogens (van Os et al. 1998,1999; Barth 1998). Van Os et al. (1998, 1999) found P. cin-namomi was Wltered out completely using slow sand Wlterswith Wne grain size (0.15–0.8 mm) at a Xow rate of 100 L/

m2/h, but passed through all other Wlters (including with aXow rate of 300 L/m2/h), while F. oxysporum, ToMV, andthe nematode R. similis could not be Wltered out com-pletely. Finer sands have a larger surface area, while lowerXow rates allow the P. cinnamomi zoospores to attach tothe grains of sand (van Os et al. 1999).

For at least some plant pathogens, the eYcacy of SSF isrelated to the concentration of inoculum in the water to betreated (Pettitt 2002). Applying water containing low con-centrations of F. oxysporum spores (103 cfu/L) resulted in100% eYcacy, while applying higher concentrations ofspores (104 or 105 cfu/L) resulted in a slight but importantreduction in eYcacy to 99.995 and 99.97%, respectively(Pettitt 2002). Researchers often use higher inoculum levelsfor ease of detection, which do not reXect realistic levels(for Fusarium, 103 cfu/L is commonly found in water, witha maximum of 8 £ 103 cfu/L), consequently giving falselylower eYcacies (Pettitt 2002). Sand Wlters were 100%eVective at removing Pythium zoospores, and 93–97%eVective at removing Fusarium spores from recirculatednutrient solutions (Ehret et al. 1999). A decline in eYciencyover time and the heavy colonization of the sand Wlters byFusarium after six months implies that it would be prudentto check Wlter eYciency annually (Ehret et al. 1999).

The eYcacy of SSF is also dependent on particle sizedistribution, the ratio of surface area to depth, and the Xowrate (Barth 1998). The Xow rate to be used is dependent onthe level and type of target propagules in the recycled irri-gation water. High levels of disease propagules or the pres-ence of small propagules, such as Fusarium microconidia,means that low rates of Xow (100 L/h/m2) should be used(Barth 1998, 1999), though Wohanka (1995) used a Xowrate of 200 L/m2/h, and removed 99.9% of all Fusariummicroconidia. If high volumes of water containing rela-tively low levels of propagules are being treated, thenhigher Xow rates can be accomodated. However, it is rec-ommended that Xow rates should not exceed 300 L/h/m2

surface area, as Wlter eYcacy against plant pathogens hasnot been determined above this rate (Barth 1998, 1999).

After SSF has been operating for about a month, a largeand diverse microbial population colonizes the high surfacearea of the sand particles (Barth 1998; Calvo-Bado et al.2003b). The colonized Wlter provides a physical barrier tothe passage of plant pathogenic propagules but also con-tains bacteria and fungi that possess antagonistic propertiesto major plant pathogens (Barth 1998). Microbial popula-tions in slow Wlters (consisting of sand or rockwool)showed a typical vertical distribution with highest densitiesin the top layer, referred to as the schmutzdecke, due totrapped organic and mineral matter serving as nutrients,with populations decreasing quickly in the Wrst few centi-meters and remaining constant thereafter (Brand and Woh-anka 2001; Calvo-Bado et al. 2003b).

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The schmutzdecke, or surface biological mat, is com-prised of a variety of organisms including algae, bacteria,fungi, actinomycetes, protozoa, rotifers, nematodes andXatworms (McNair et al. 1987; Brand and Wohanka 2001;Lloyd 1973; Ellis 1985; Huisman and Wood 1974; Duncan1988), and in particular the type of algae present is impor-tant for Wlter performance (Ridley 1967; McNair et al.1987). When Wlamentous algae predominate, the schmutz-decke exhibits high tensile strength, increasing the rate ofWltration and decreasing Xow resistance (McNair et al.1987). The eYcacy and consistency of SSF may beimproved either by adding selected organisms to the natu-rally suppressive population of microorganisms, or bymanipulating the environment to encourage the prolifera-tion of desirable members of the population (Calvo-Badoet al. 2003b). However, adding a suspension of actinomy-cetes, which are suggested to play a role in disease suppres-sion, to the recirculating nutrient solution for a cucumbercrop, did not cause signiWcantly less disease due to P.aphanidermatum (van Os et al. 2004). McNair et al. (1987)investigated the eVect of adding a naturally occurringammonium-selective zeolite mineral termed clinoptiloliteas a surface amendment to the Wlter of an SSF system andfound that the removal of particles (not speciWcally plantpathogenic propagules) from raw river water was improvedcompared to unamended Wlters.

In ascertaining the signiWcance of the biological compo-nent of slow sand Wlters, Brand and Wohanka (2001)showed that biologically activated slow sand Wlters weresigniWcantly more eVective than sterilized Wlters againstX. campestris pv. pelargonii, but there was no diVerenceagainst F. oxysporum f. sp. cyclaminis. It has been shownthat passing recycled nutrient solutions through a slow sandWlter causes a shift in population diversity of the naturalmicroXora (van Os and Postma 2000). Numbers of Xuores-cent pseudomonads, Wlamentous actinomycetes and fungiwere signiWcantly lower in the SSF eZuent than in theinXuent, but numbers of total aerobic bacteria were similar(up to 10% reduction) after slow sand Wltration, and thismay have ramiWcations for the disease suppressiveness ofthe natural microXora (van Os and Postma 2000).

The recommended temperatures for optimal biologicalactivity in slow sand Wlters are around 10–20°C (Pyper andLogsdon 1991). There are conXicting reports on the eVectof lower temperatures, such as 2–5°C. Ufer et al. (2008)and Calvo-Bado et al. (2003a) ascertain such temperaturesdo not seem to impede Wltration success, yet Van Kuik(1994) suggests they reduce the eYcacy of slow sand Wltra-tion. Conversely, warmer temperatures, above 20°C, lead toexcellent biological activity in the Wlters, but as tempera-tures increase, the dissolved oxygen concentrationdecreases, and this can begin to limit eYcacy (Pyper andLogsdon 1991). In addition, this may increase the risk of

higher populations of Legionella developing (Calvo-Badoet al. 2003a). To ensure that the microXora on the schmutz-decke are not exposed to large temperature and moistureXuctuations or other disturbances, the Wlter design shouldallow for a continual head of recirculating water on top ofthe Wlter of a minimum depth of 100 mm, and Wlter mediadepth should be maintained at a minimum of 80 cm (Barth1998).

As an additional treatment to control any undesirablemicrobes which may have breached the Wlter, some systemsinject sodium hypochlorite (3–5 ppm) into the Wltrate (Ng1999).

Certain disadvantages of sand make the investigation ofalternative media desirable (Barth 1998). Sand is heavy,making it diYcult to construct or move the Wlter system,and sand Wlters can become clogged quickly due to Wneinorganic particles or peat (Wohanka and Helle 1996).

Rockwool Granulated rockwool has been demonstrated asthe most eYcient Wlter material for the removal of the bac-terium X. campestris pv. pelargonii (compared to sand,pumice, and anthracite) (Wohanka et al. 1999), and the fun-gus F. oxysporum f.sp. cyclaminis (compared to sand, pum-ice and Seramis®) (Wohanka and Helle 1996). Althoughbeing about four times the price of sand, rockwool hasimportant advantages over sand as a Wlter medium: it has amuch lower (ten fold) speciWc density enabling easier con-struction and relocation of the Wlter; it does not require sev-eral layers of gravel to prevent clogging, enabling the Wlterunit to be smaller in size; and tends to clog less, saving onmaintenance costs (Wohanka and Helle 1996; Wohankaet al. 1999).

A granulated rockwool product, marketed as “Grodan®”,claims various additional advantages as a slow Wltrationmedium over sand in that it has much greater surface area,has greater uniformity, does not require regular removal ofthe top layer of the Wlter (Chin 2005), and is more eVectiveat removing Fusarium (S. Featherston, AIS Greenworks P/L, pers. comm.). A Xow rate of 100–150 L/m2/h is recom-mended and should be monitored constantly (S. Feather-ston, AIS Greenworks P/L, pers. comm.). However, theGrodan® system does not guarantee total removal of patho-gens but reduces their level substantially (S. Featherston,AIS Greenworks P/L, pers. comm.).

Pumice Pumice granules (lava grains) have been used asa substrate in slow Wlters (Ufer et al. 2008). This systemremoved Phytophthora spp. from recycled irrigation waterin commercial ornamental nurseries, with Xow rates twiceas fast as in slow sand Wltration (Ufer et al. 2008). This sys-tem also removed Pythium zoospores with 100% eYcacyand Fusarium spores with 99% eYcacy from recirculatednutrient solutions (Ehret et al. 1999). Pumice Wltration costsabout three times as much as slow sand Wltration, for 1 m3

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of Wltered water, but was comparable to other disinfectionmethods such as heat treatment, UV irradiation, ultraWltra-tion, ozonation, iodine, and hydrogen peroxide (Ufer et al.2008). The recommended temperatures for optimal biologi-cal activity are 15–25°C, but temperatures of 5°C did notseem to impede Wltration success (Ufer et al. 2008; Le Quil-lec et al. 2005). Compared to slow sand Wltration, pumiceWltration saves on space due to its higher Wltration capacitybut is a more complex system, with repairs requiringtrained specialists (Ufer et al. 2008).

Other Filter media have a signiWcant eVect on the eYcacyof slow Wltration, and several other alternatives to sandhave been investigated. Grains of pozzolana, a Wne sandyvolcanic ash, have been used as a substrate in slow Wlters(Déniel et al. 2004). This system removed F. oxysporumfrom the recirculated nutrient solution, with eliminationenhanced signiWcantly after biological activation of theWlter with selected bacterial strains (Déniel et al. 2004).

In one study investigating alternative media, activatedcharcoal was the most eYcient Wlter material, eliminating92.5% of F. oxysporum propagules, compared to sand(82.3%), silica (90.8%), vermiculite (90.5%), and perlite(50.4%) (Park et al. 1998). Similarly, Wohanka and Helle(1996) investigated the eYcacy of porous clay granules(Seramis®) and pumice at removing F. oxysporum f. sp.cyclaminis and found that not only were these media moreexpensive than sand, but no advantage was gained in rela-tion to the construction and relocation issue, and mostimportantly, they were less eYcacious than sand and rock-wool. A material called Siran (sintered glass) was 100%eVective at removing another pathovar, F. oxysporum f. sp.pisi, but it is prohibitively expensive (Wohanka 1995).

In another study, glass wool, rockwool, and polyure-thane foam were, in general, as eVective as sand at remov-ing F. oxysporum and X. campestris, but the authorscautioned that other factors such as cost, ease of handlingand transport must be considered before any medium couldbe recommended above sand (van Os et al. 2001). Gravelhas also been compared as a Wlter medium to sand andpumice for its eYcacy to remove Pythium and Fusariumpropagules from recirculated nutrient solutions (Ehret et al.1999). Gravel Wlters were 100% eVective (as were sand andpumice), at removing Pythium zoospores, but only 93–97%eVective at removing Fusarium spores (as eYcacious assand but not as good as pumice with 99% eYcacy) (Ehretet al. 1999).

Membrane Various membrane Wlters can be used toremove plant pathogenic propagules from recycled water.Pore sizes in membrane Wltration systems diVer, withmicroWltration removing particles ¸50 nm, ultraWltrationremoving particles ¸3 nm, and hyperWltration (or reverse

osmosis) removing particles ¸0.1 nm. Many authors agreethat the elimination of microorganisms from recycled irri-gation water using membrane Wltration systems is probablynot practicable due to high installation costs, pumpingcosts, downstream processing costs, and rapid clogging ofthe expensive Wlters (Pettitt 2003; Downey et al. 1998;Rolfe et al. 2000; Runia 1995; Lesikar et al. 1997). How-ever, Tu and Harwood (2005) reported that the Wlter sys-tems they used to remove Pythium zoospores fromrecirculating nutrient solution were highly eYcacious, eco-nomical and needed minimal infrastructure compared toother disinfestation systems. The authors found two veryeVective Wlters: (1) a membrane module Wlter consisting ofmany hollow Wber membrane strands with a porosity of0.01 �m (ultraWltration), which completely removed zoo-spores and bacteria; and (2) a sediment Wlter cartridge com-posed of pleated cellulose/polyester materials with aporosity of 0.5 �m (microWltration), which completelyremoved zoospores, but not bacteria. Both Wlters withstoodpressure up to 2.5 kg/cm2 delivered a Xow rate of 50 L/min,and their life span was increased with preWltration using aWlter of larger pore size and strainer (Tu and Harwood2005). Liu et al. (1999) used similar ultraWltration Wlters toremove tomato mosaic virus (ToMV) from greenhousewastewater, while Ohtani et al. (2000) used similar micro-Wltration Wlters to remove P. solanacearum.

Filtration has also been assessed as a control method forPythium root rot of hydroponically grown cucumbers(Goldberg et al. 1992; McPherson et al. 1995). In the studyby Goldberg et al. (1992), a 7-�m Wlter was eVective atremoving zoospores of P. aphanidermatum from infestedwater. In the study by McPherson et al. (1995), two Wltra-tion modules each housing 0.2-�m Wlters were eVective atpreventing widespread dispersal of P. cryptogea andP. aphanidermatum in recirculated hydroponic solutions.Some nurseries use sand-Wlled canisters to Wlter out largeparticles, and limited sampling of resulting Wltrates has sug-gested that this reduces the number of viable Pythium andPhytophthora propagules by a factor of 2–10 (MacDonaldet al. 1994). Repeated exposure of plants to such low levelsof inoculum could still represent a disease risk, thoughthere are few studies to support this premise (MacDonaldet al. 1994).

Heat

Heat treatment is currently the most commonly usedmethod for disinfesting recycled nutrient solutions in theNetherlands (van Os 2000). The recycled water is passedthrough two heat exchangers where it is heated to 95°C for30 s (Newman 2004). Water is pumped into the Wrst heatexchanger and is preheated using the heat lost from waterthat has already been through the system. Then the water is

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pumped into the second heat exchanger to heat to therequired disinfestation temperature (Yiasoumi 2005). Todisinfest 10,000 L of irrigation water, about one gigajouleof gas is required (Yiasoumi 2005; Rolfe et al. 2000). Thecost of gas varies around the world, so in some countries,this method is prohibitively expensive. Besides large infra-structure and high energy costs, other disadvantagesinclude that this method kills pathogens and beneWcialmicrobes indiscriminately; it may have undesirable eVectson some chemical compounds; and it requires cooling ofthe water before use (Tu and Harwood 2005; van Os andAlsanius 2004).

This method is eVective in controlling numerous patho-gens including Pythium (Rey et al. 2001; Runia andAmsing 2001), Phytophthora (Runia and Amsing 2001),F. oxysporum, Verticillium dahliae (Runia and Amsing2001), the nematode R. similis (Runia and Amsing 2001),the bacterium Erwinia chrysanthemi (Runia and Amsing2001), tobacco mosaic virus (TMV), and tomato mosaicvirus (ToMV) (Runia et al. 1988; Runia 1995). However,due to the prohibitive cost of achieving such a high temper-ature (Pettitt 2003; Poncet et al. 2001), it has been recom-mended subsequently that water is heated to only 60°C for2 min, which translates to a 42% reduction in energy use(Runia and Amsing 2001) and still eliminates plant patho-genic fungi, fungal-like organisms, bacteria and nematodes.Water should be heated to 85°C for 3 min if virus diseasesare a potential problem in the crop to be grown (Runia andAmsing 2001). In addition, it is recommended that the pHof the water is reduced to 4.5, since this prevents calciumprecipitation on the metal heat exchange plates (Newman2004). Also corrosion-free materials such as stainless steeland synthetic materials must be used (a further cost), sinceequipment containing copper and zinc can deteriorate andbe phytotoxic (Runia et al. 1988).

There has been further research into the disinfestationeYcacy of lower, more practically achievable, tempera-tures. Steinberg et al. (1994) used a wet condensationheater to kill fungi after 30 s at 59°C, and most bacteriaafter 45 s at 65°C. Complete removal of virus particles wasmore elusive, but their number was reduced greatly,thereby reducing the disease potential. A combined eVect ofboth temperature and UV irradiation from the Xame wasthought to contribute to the eYcacy of the heater (Steinberget al. 1994). Ahonsi et al. (2007) reported that zoosporerelease by Phytophthora nicotianae was completely inhib-ited at 36–38°C and suggested that heating recycled irriga-tion water may reduce disease caused by Phytophthora spp.(and possibly Pythium spp.). The use of such low tempera-tures may obviate the problematic and costly need for cool-ing before re-using the water for irrigation (Brockwell andGault 1976; Ehret et al. 2001; Runia 1995; Runia et al.1988). MacDonald et al. (1997) suggested that heating

recycled water (via an heat exchanger, solar power or acombination of both) to 45°C could be an eVective meansof disinfesting small volumes of water.

A variation on heat treatment is Xame disinfection,which gives excellent control of fungi but poor control ofviruses (van Meggelen-Laagland 1996). In this treatment,preWltered water is pumped into a heat exchanger, where itis heated using the heat lost from water that has alreadybeen through the system. The water is then sprayed into asecond chamber where it is exposed to a gas Xame, UVlight, and infrared light for 16 s.

Ultraviolet (UV) light

UV treatment systems usually consist of a cylindrical ves-sel (reactor) with UV lamps mounted centrally within, withthe water to be treated Xowing through the annulus betweenthe lamps and the vessel wall (Downey et al. 1998). TheUV lamps emit UV-C radiation at 254 nm (Newman 2004).Microorganisms absorb most of the energy at this wave-length, altering their DNA and RNA, thereby killing theseorganisms. The eYcacy of disinfestation is dependent onduration and intensity (or dose). A UV dose of 100 mJ/cm2

is recommended for removing pathogenic fungi, but higherdose of 250 mJ/cm2 is required to remove all organismsincluding viruses (Runia 1994b, 1995). An even higherdose of 500 mJ/cm2 was required to achieve 96% mortalityof the nematode R. similis, but a dose of 100 mJ/cm2 pre-vented reproduction and, importantly, infection of plantroots (Amsing and Runia 1995). Ultraviolet irradiation hasbeen used to reduce populations of various species of Phy-tophthora, Pythium, Alternaria, Colletotrichum, Fusarium,bacteria, and nematodes in contaminated irrigation water(Grech et al. 1989; Amsing and Runia 1995; Banihashemiet al. 1992; Fitzell and Peak 1990; Rey et al. 2001; Mebaldset al. 1997b). In an Australian study, UV light eVectivelycontrolled a range of fungal pathogens of cut Xower cropsand nursery plants (Mebalds et al. 1997b; James et al.1995b), was most eVective against P. cinnamomi zoo-spores, had intermediate eYcacy on F. oxysporum and Col-letotrichum capsici, and was least eVective againstAlternaria zinniae. Fusarium solani was more susceptibleto UV irradiation than was Alternaria alternata, perhapsdue to the production and accumulation of speciWc proteins(Osman and Abo-Zeid 1987).

In addition to dose, disinfestation eYcacy is also depen-dent on the type of reXector, penetration depth, and Xowrate of the water (Rolfe et al. 1994), with low Xow ratesbeing more eVective at controlling pythiaceous species(Cohn and Hong 2003). However, the most important fac-tor aVecting eYcacy is water clarity. UV light is reXectedoV or absorbed by any material in the water such assuspended solids, plant debris, and potting media, and

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consequently, Xocculation and Wltration prior to treatmentis essential (Newman 2004; Runia 1994b; Adams andRobinson 1979; Grech et al. 1989). In water with high UVtransmission, a pathogenic propagule Xowing through thevessel will be exposed constantly to UV radiation, with theaccumulated UV dose (UV radiation x time) dependentsolely on the time the propagule spends in the reactorchamber. Conversely, in water with low UV transmission, apathogenic propagule Xowing through the vessel will beexposed intermittently to UV radiation, with dissolved sol-ids and suspended organic and inorganic materials fre-quently shielding the propagule (Downey et al. 1998). As aresult, the accumulated UV dose depends strongly on posi-tion of the propagule in relation to these shielding factorsand the time spent at each position. Therefore, recycled irri-gation water with high levels of suspended and dissolvedmaterials prevent adequate UV disinfection by reducing thetotal dose delivered (Downey et al. 1998).

For UV radiation to eVectively disinfest recycled irriga-tion water, a minimum UV transmission rate of 60% isessential (Mebalds et al. 1996). Of twenty-nine nurseriessurveyed in a 1996 Australian study, less than 25% hadwater with eVective UV transmission rates (over 60% trans-mission), while 62% of properties had water with ineVec-tive UV transmission rates (less than 50% transmission)(Mebalds et al. 1996; James et al. 1995b). Downey (1997,cited in Downey et al. 1998) suggested that UV transmis-sion rates in the USA are often as low as 10%. Unfortu-nately, Wltering can sometimes do little to improve the UVtransmission rate, since it is dissolved solids that are themain absorbers of UV radiation (Mebalds et al. 1996).

Other UV sources have been used for the treatment ofrecycled irrigation water. A pulsed-UV laser source (nar-row-band UV radiation) seemed more eVective at killingzoospores of various Phytophthora spp. than UV lamps(wide-band, continuous UV radiation) (Banihashemi et al.1992). Not surprisingly, less UV was required to kill propa-gules in distilled water than in recycled nursery water, pre-sumably due to the latter having soluble organic materialsand the presence of suspended solids. In similar experi-ments, a Hg-vapor lamp did not possess suYcient energy tokill spores in wastewater that contained dissolved organics(MacDonald et al. 1997). However, two pulsed UVsources, an excimer laser and a xenon Xashlamp, possessedthe power levels required but only with the laser was therepetition rate high enough to reliably treat large volumesof water.

The advantages of UV treatment include that it is non-corrosive, not dependent on pH, and does not require theaddition of chemicals to the water, which can form highlyreactive radicals that react with organic matter in the waterto form toxic compounds (Grech et al. 1989; Adams andRobinson 1979).

A couple of potential disadvantages to UV treatment ofrecycled irrigation water have been identiWed. High inten-sity UV treatment of recirculating nutrient solutions cansigniWcantly inhibit the growth of plants downstream of thetreatment (Schwartzkopf et al. 1987). It is believed to bedue to the generation of ozone and/or free radicals in thenutrient solution from the UV treatment (Blaqka and Proc-házková 1983; Schwartzkopf et al. 1987; Vanachter et al.1988). Also, UV irradiation can destroy iron chelate(Daughtrey and Schippers 1980), precipitating iron that cancoat onto the UV tube, reducing UV penetration, and result-ing in iron chlorosis if iron levels are not amended aftertreatment (Stanghellini et al. 1984; Schwartzkopf et al.1987; Tu and Harwood 2005; Tu and Zhang 2000). How-ever, Acher et al. (1997) found that iron chelates diVer intheir stability when exposed to UV, and some may have abeneWcial eVect on plant growth, depending on the plantspecies. Other potential disadvantages include soluble ironrestricting UV penetration resulting in non-uniform deliv-ery; turbulence is required to maximize exposure of thesolution to UV; the UV system is costly, requiring highmaintenance levels; and UV lamps degrade with time,which results in a reduced dose (Tu and Harwood 2005).Estimates of this reduced output with age are up to a 10%loss after 1,000 h of operation (Rolfe et al. 2000) and a 35%loss after continuous operation for a year (Adler andWilson 1999). Thus, UV lamps need to be monitored andchanged as required.

Also, there have been instances of increased spread ofdisease from infected plants introduced downstream of UVtreatment, possibly due to non-target eVects causing a dropin natural disease suppression (Pettitt 2003). Zhang and Tu(2000) found a signiWcant reduction in Pythium populationsin UV-treated solutions, but not a decrease in root rotcaused by this pathogen. Additionally, the authors found areduction of non-target bacterial populations in the UV-treated solution and suggested this led to a subsequentreduction of populations in the rhizosphere, and that thispossibly reduced the natural suppression of pathogen activ-ity (Zhang and Tu 2000).

Other

Pressure Pressure may play a role in reducing the viabil-ity of plant pathogens in recycled irrigation water (Bankoet al. 2004; Heald and Johnson 1969). Water recycled fromretention ponds and discharged from irrigation risers con-tained less viable Phytophthora inoculum than water col-lected directly from such ponds (Banko et al. 2004). Bankoet al. (2004) inoculated Catharanthus roseus plants withzoospore suspensions at application pressures of 0, 21, 42,or 63 mPa, applied using a CO2-pressurized sprayer, andfound that there was a signiWcant linear reduction in disease

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with increased application pressure, suggesting pressuremay be a factor in reducing inoculum viability. However,the authors stated that other possible factors were underinvestigation, and later work by Ahonsi et al. (2008, 2010)showed that exposure to CO2 killed zoospores in water,with pressure having no eVect on zoospore viability orinfectivity. However, pressure did have a facilitating eVect,with the greater the pressure, the higher the level of dis-solved CO2. Similarly, Heald and Johnson (1969) foundnematodes in irrigation water but observed they were notcapable of infecting susceptible plants after passing throughthe overhead irrigation system, probably due to the pressureat the pump or the sprinkler oriWce.

Sonication Sonication is the application of ultrasoundenergy to agitate particles and can be used for disinfestationsince it mechanically disrupts microbial cells, causing death(Tu and Zhang 2000). Sonication for 1.5 min destroyed allP. aphanidermatum propagules in suspension, but only25% of beneWcial bacterial cells with disease-suppressivequalities, so this method has potential for selective control.For disinfestation eYcacy, sonication compared favorablyto heat and UV. However, sonication is ineYcient anduneconomical on a commercial scale, with issues includingthe high cooling requirement for the sonication device thatis diYcult to achieve, the slow Xow rate that is limited bycapacity, and the delicateness of the vibration mechanism(Tu and Harwood 2005).

Electrostatic precipitation Electrostatic precipitation usesa form of radionic or eloptic energy, so-called because ithas both electrical and optical properties, to precipitate outundesirable pathogens via rearrangement of electrons inwater (Wilkerson 2000). No further information could befound on this technique.

Chemical

Prior to applying any chemical treatments to disinfest recy-cled irrigation water, the water should be Wltered. Thisremoves organic matter and a substantial portion of themicrobial population, therefore lowering the chemicaldemand of the water (De Hayr et al. 1994). Similarly, theaddition of nutrients to the water for fertigation should bedone following chemical disinfestation, after the treatmenttime has elapsed, since some nutrients, such as ammonium,can react with treatment chemicals (De Hayr et al. 1994).An added beneWt of chemically treating irrigation waterincludes algae removal from irrigation sprinklers and pipes,paths and drains (Lake 2000). Blockages of irrigationequipment due to algal growth are common and can lead touneven watering and poor plant health, which equates tolost revenue. A disadvantage is that chemicals have a detri-

mental eVect on beneWcial organisms (Ufer et al. 2008),causing a microbial imbalance, allowing pathogens tofreely colonize the system, as there is little competition(Postma 2004).

Chlorine

Chlorine can be used for disinfestation of recycled irriga-tion water in liquid, solid, or gaseous forms (Clark andSmajstrla 1992). Liquid chlorine, as sodium hypochlorite,is the most common type of chlorine used. In water, sodiumhypochlorite forms a hypohalous acid called hypochlorousacid (HOCl); a strong oxidizing agent responsible for thebiocidal activity (De Hayr et al. 1994). Hypochlorous acidreacts with proteins in the microbial cells, disrupting essen-tial metabolism (De Hayr et al. 1994). Besides hypochlo-rous acid, hydroxyl ions (OH¡) are also formed, whichcause an increase in the pH of the water (Clark andSmajstrla 1992; De Hayr et al. 1994). Hypochlorous aciddissociates into hydrogen ions (H+) and hypochlorite ions(OCL¡) and as the pH rises, dissociation is favoured(Anonymous 2007). As a result, at pH 6, 96% of the solu-tion is in the HOCl form, the most active and desired statefor disinfestation. But at pH 7, 73% is as HOCl; at pH 8,only 22% is as HOCl (Clark and Smajstrla 1992); at pH 8.5,only 7% is as HOCl (Pearch and OliV (2005), cited inAnonymous 2007); and at pH 10, only 3% is in the HOClform and the solution is completely ineVective as a disin-fectant (Shield 2001; Anonymous 2007). From this, it isobvious why chlorination is inadequate if the pH of thewater is above 7.5 and ineVective above 8.5 (Mebalds et al.1996; Yiasoumi et al. 2005). For maximum microbiocidaleVectiveness, a pH 5–6 is recommended (Shield 2001), andsince runoV water from nurseries can often have a pHabove 7.5, acidiWcation is necessary prior to chlorination(Rolfe et al. 2000; Mebalds et al. 1996; Lesikar et al. 1997).

Solid chlorine, as compressed calcium hypochloritepowder, can also be utilized for disinfestation. It is installedas slow release blocks into disposable cartridges (S. Woods,Klorman Industries P/L., pers. comm.) and when it is dis-solved in water, HOCl and OH¡ are formed (Chin 2005;Clark and Smajstrla 1992). Installation of this system isinexpensive and simple, is safer to use than chlorine gas, isless phytotoxic than sodium hypochlorite, is less corrosiveto pipes and equipment (Chin 2005), and the calcium isavailable for uptake by the plant (S. Woods, KlormanIndustries P/L., pers. comm.). However, it is more costly torun and needs constant monitoring (Chin 2005).

Inline injection of chlorine gas into recycled irrigationwater leads to the formation of HOCl and hydrochloric acid(HCl) (Clark and Smajstrla 1992; Daughtry 1984). Thismethod provides the disinfectant in its cheapest and mostconcentrated form, however, there are serious associated

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safety issues, as it is a respiratory irritant aVecting themucous membranes and can be fatal at high concentrations(Clark and Smajstrla 1992). Therefore, this method of chlo-rination is not recommended (Mebalds et al. 1996). Grechand Rijkenberg (1992) used an electrolytic method of chlo-rine gas generation to successfully eradicate populations ofPhytophthora, Fusarium, algae, and protozoa and reducebacterial populations in irrigation water, but this treatmenthad no eVect on nematode populations.

Despite chlorination being a popular method of disin-festing nursery irrigation water, De Hayr et al. (1994) pro-posed this method is not being used to its full capability bymany nursery operators. The authors suggested that thiswas mainly due to a lack of understanding of the impor-tance of routinely monitoring chlorine demand, to ensurethe constant maintenance of eVective concentrations of freeavailable chlorine (De Hayr et al. 1994). While manymicrobial plant pathogens are controlled by a free residualchlorine concentration of 1–3 ppm, higher initial levelssuch as 5–10 mg/L are required to compensate for theintrinsic chlorine demand of diVerent water sources (Clarkand Smajstrla 1992; De Hayr et al. 1994; Ewart andChrimes 1980; Daughtry 1984). Chlorine reacts with varioussubstances in water, including ferrous ions, ammoniumions, and other inorganic and organic contaminants, makingthe chlorine unavailable for disinfestation (Clark and Sma-jstrla 1992; De Hayr et al. 1994; Daughtry 1984). Forinstance, hypochlorous acid reacts with iron in solution,oxidizing ferrous ions to insoluble ferric hydroxide, form-ing a precipitate, and using up available chlorine in the pro-cess (Clark and Smajstrla 1992).

Recycled irrigation water contains various and Xuctuat-ing levels of ammonium ions and other nitrogen-basedcompounds. Chloramine is readily formed when chlorinereacts with these nitrogenous compounds. While chlorine isa very eVective biocide, chloramine is very poor by com-parison, being about 80 times less eVective (Johnson andOverby 1971; White 1999; De Hayr et al. 1994) and ismore phytotoxic than chlorine, though most plants tolerateconcentrations up to 2.9 mg/L (Skimina 1992; Date et al.1999). However, the reaction with ammonia is not immedi-ate, and within this brief period of initial elevated levels offree chlorine, there is an increased rate of disinfection lead-ing to the control of many pathogens (Daughtry 1984).

Chlorine demand diVers with the type and amount oforganic and inorganic material in the recycled irrigationwater, which itself can vary greatly with location and sea-son (Hong et al. 2003c). As a result, the chlorine demandcan be as high as 25–30 mg/L (De Hayr et al. 1994). It isessential to monitor the free residual chlorine concentrationto ensure eYcacy of the treatment. Despite recycled irriga-tion water being treated with a chlorine gas injection sys-tem prior to pumping into irrigation risers, Bush et al.

(2003) was able to recover various species of Phytophthoraand Pythium using Wltering assays and baits. Also, patho-gens residing in plant debris are protected from chlorinedisinfestation. Therefore, to maximize chlorinationeYcacy, recycled irrigation water should be allowed tostand to allow sedimentation or Wltered prior to treatment(Steadman et al. 1979).

Besides the inorganic and organic matter content, theeYcacy of chlorination also varies with the following fac-tors: pathogen type, pathogen load, and the pH and temper-ature of the water (being more eYcacious at highertemperatures) (Hong and Moorman 2005; Phillips andGrendahl 1973; Segall 1968). The eVective chlorine dose(concentration x exposure duration) is dependent on the tar-get pathogen. In a recent study, all chlorine concentrations(0.5–30 mg/L) and exposure durations (30 s–30 min) testedgave 100% kill of Colletotrichum, Fusarium, and Rhizocto-nia propagules (Anonymous 2007). Similarly, most chlo-rine concentrations and exposure durations controlledCylindrocladium, Alternaria, and Botrytis except some ofthe lower concentrations and shorter exposure durations.This same study also compared the eYcacy of chlorinedioxide, bromine, and chlorine/bromine to that of chlorineand found chlorine was the most eYcacious for controllingthe fungal plant pathogens tested (Anonymous 2007).

Chlorine sensitivity can vary with genera, species, path-ovar, and even type of propagule of a single pathogen(Hong et al. 2003c). The free chlorine threshold and thecritical contact time at which there was no detection of thepathogen diVered between fungal genera and species(Cayanan et al. 2009b). Cayanan et al. (2009b) assessedchlorine as a disinfectant for Wve common nursery patho-gens, namely Phytophthora infestans, Phytophthora cacto-rum, Pythium aphanidermatum, F. oxysporum, and R. solani,in irrigation water. A free chlorine concentration of 2.5 mg/L was required to control pythicaeous species only, but ahigher free chlorine concentration of 14 mg/L was requiredfor the control of all Wve pathogens (Cayanan et al. 2009b).However, such a high free chlorine concentration is phyto-toxic to common nursery species (Cayanan et al. 2008).Severe phytotoxic eVects included necrotic mottling, leafnecrosis and chlorosis, stunting, and premature leaf abscis-sion, thus reducing the marketability of the plants (Cayananet al. 2008; Frink and Bugbee 1987). Therefore, the authorssuggested if only pythiaceous species are commonly caus-ing disease in nurseries, free chlorine concentration of 2–2.4 mg/L can be used with minor phytotoxic (plants stillmarketable) or no phytotoxic eVects (Cayanan et al. 2008,2009a; Hong et al. 2003c). Alternatively, designing an irri-gation system where the high levels of free chlorine areremoved from the water before irrigation, either by aera-tion, activated carbon, or treatment with sodium sulWte orsodium metabisulphite, would avert phytotoxicity

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(Cayanan et al. 2009b; Runia 1989; White 1999). Similarly,Price and Fox (1984) found that eYcacious doses of chlo-rine (as sodium hypochlorite) were phytotoxic. They used5 mg/L of available chlorine for 5 min to kill propagules ofF. oxysporum f. sp. dianthi in a recirculating nutrient Wlmhydroponic system, but because daily applications wererequired to kill any new inoculations, sodium accumulatedto a phytotoxic level.

The eVect of chlorine concentration on the survival ofzoospores of P. nicotianae and Pythium spp. has beendetermined (Hong 2001; Hong and Richardson 2004). Zoo-spore survival was reduced with increasing concentrationsof chlorine, and no zoospores survived at 4 ppm free chlo-rine for P. nicotianae, or at 2 ppm for 11 of 15 isolates ofPythium spp. (Hong 2001; Hong and Richardson 2004).Lang et al. (2008) suggested using oxidation reductionpotential (ORP) as a reliable real-time measurement of theoxidizing, and so disinfesting, ability of a chlorine solution.The authors recommended maintaining ORP values of achlorine solution >780 mV to kill Pythium zoospores (Langet al. 2008). They also suggested lowering the pH of thewater to 6 to achieve maximal disinfestation of Pythium,since lowering the pH increases ORP values. Newman(2004) suggests that an ORP value of 650 mV is the mini-mum threshold for typical antibacterial activity.

Chlorine has also been used to control bacterial plantpathogens (Lacy et al. 1981; Poncet et al. 2001). Erwiniaspecies suspended in sterile distilled water, pond water,creek water, or well water were subjected to various con-centrations of sodium hypochlorite for 1 min. The source ofthe irrigation water aVected the eYcacy of chlorination,with eYcacy reduced in pond or creek water, probably dueto the binding of chlorine to dissolved and suspended inor-ganic and organic materials (Lacy et al. 1981). An activechlorine concentration of 4 mg/L for 30 min was requiredto disinfest recycled irrigation water of Agrobacterium tum-efaciens (Poncet et al. 2001), though it is not reportedwhether lesser concentrations or shorter exposure timeswere tested.

Chlorine has been investigated for its eYcacy to controlviral plant pathogens. While one study found 4 ppm ofhypochlorite for 30 min eVective at eradicating cucumberleaf spot virus (CLSV) inoculum (Rosner et al. 2006),another study found cucumber green mottle mosaic virus(CGMMV) particles were still infective after exposure to5 mg/L of chlorine for 2 h (Runia 1989). Chlorine has alsobeen investigated for its eYcacy to control root-knot nema-todes. Hatching was reduced in eggs exposed to 50,000 or125,000 �g available chlorine/mL for ¸1 h (Stanton andO’Donnell 1994). Second-stage juveniles exposed to ¸2 �gavailable chlorine/mL for ¸24 h lost their motility and theirability to produce galls (Stanton and O’Donnell 1994).Post-plant applications were not eVective in controlling

established infections of root-knot nematode in hydroponicsystems, but pre-plant applications (4 weeks before plant-ing) of ¸4 �g available chlorine/mL to the nutrient solutioncontrolled root-knot nematode.

The popularity of chlorination is, in part, due to it beingeconomical to set up (Hong et al. 2003c). However, ongo-ing running costs are expensive compared to many otherdisinfestation methods (Rolfe 2001). An added bonus ofchlorination is the formation of a stable residual that assistsin cleaning algal or bacterial slime out of the irrigation sys-tem (Yiasoumi 2005). A major disadvantage of using chlo-rine is that it produces long-lived by-products, such astrihalomethanes, adsorbent organic halogens, and chloram-ines, which have potential environmental and human healthimpacts, including carcinogenic and mutagenic properties(De Hayr et al. 1994; Stewart et al. 2001; Anonymous1998; Bull et al. 1990). As a result, the release of watercontaining these by-products to the environment is strictlyregulated in some countries, such as the USA.

Chlorine dioxide

Chlorine dioxide is an eVective biocide for the treatment ofplant pathogens in recycled irrigation water due to itspotency as an oxidant, being more than twice as powerfulas chlorine (Sussman and Rauh 1978), and reportedly 25times more eVective than chlorine in its gaseous form(Newman 2004). Chlorine dioxide does not dissociate andremains chemically unchanged in water of pH 4–8.4 andalso does not react with nitrogen, unlike chlorine that losesits biocidal properties in water with a pH of 7.5 and aboveand when it reacts with nitrogen to form chloramine(Armitage 1993). The eYcacy of chlorine, chlorine dioxide,and a bromo-chloro compound were compared for the con-trol of zoospores and chlamydospores of P. cinnamomi inrecycled irrigation water (Armitage 1993). Chlorine diox-ide was the most eVective treatment method over all pHvalues and contact times evaluated, with a concentration of0.5 ppm in contact for 2 min required to control zoospores,and a concentration of 1 ppm in contact for 2 min requiredto control chlamydospores (Armitage 1993).

The eVective chlorine dioxide dose (concentration xexposure duration) is dependent on the targeted fungalpathogen. In a recent Australian study, chlorine dioxidewas most eVective against Colletotrichum, causing 100%kill at concentrations of 5, 10 and 30 mg/L for all exposuredurations (Anonymous 2007). The biocide was slightly lesseVective against Cylindrocladium and Fusarium, giving90–100% control and 70–100% control, respectively, at 10and 30 mg/L for all exposure durations. Control of Alter-naria was uneven and poor, and control of Botrytis wasonly achieved with the highest concentration. Chlorinedioxide was ineVective against Rhizoctonia (Anonymous

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2007). When compared to other chemical disinfestationmethods including chlorine, while chlorine dioxide waseVective in general, chlorine gave superior control acrossthe fungi tested.

In earlier studies, chlorine dioxide eVectively controlleda range of fungal pathogens of cut Xower crops and nurseryplants (Mebalds et al. 1997b; Mebalds et al. 1996).Mebalds et al. (1997b) found that as little as 2.6 ppm chlo-rine dioxide for 2 min was required to kill zoospores of P.cinnamomi, but a higher concentration for longer exposuretime (8.9 ppm for 4 min) was needed to kill chlamydosp-ores of the same species. Pythium ultimum oospores werecontrolled after exposure to 1.2 ppm chlorine dioxide for2 min in tap water but required a longer exposure to a moreconcentrated solution (4 min in 2.4 ppm) for control in damwater. Colletotrichum capsici was controlled at 2 ppmchlorine dioxide for 2 min, while F. oxysporum required1 ppm chlorine dioxide for 4 min. Alternaria zinniae sporeswere more resistant, only controlled in tap water after an8 min exposure to 3.1 ppm chlorine dioxide. Mebalds et al.(1996) reported that spores of all fungi (namely P. cinnam-omi, F. oxysporum, C. capsici, P. ultimum, and A. zinniae)in dam water were killed with chlorine dioxide at 3.3 mg/Land exposure durations of less than 10 min (Mebalds et al.1996). With a pH of 10, there was no reduction in the treat-ment eYcacy, so this treatment method seems very usefulin Australian nurseries that generally have high pH levels intheir recycled water (NGIA 2005). For example, of 29 nurs-eries surveyed, most had a pH too high for eVective chlori-nation on at least one occasion (James et al. 1995b). Thereis a lack of data on phytotoxicity thresholds for chlorinedioxide and its constituent chlorite ions, and further work isrequired to examine its eYcacy on other important plantpathogens, such as other fungi, bacteria, and nematodes(NGIA 2005; Mebalds et al. 1996; Yiasoumi et al. 2005).

The instability of chlorine dioxide as a gas demands thatit is produced and used at the same location requiring spe-cialized equipment, but it is then stable and soluble in water(Newman 2004). Another disadvantage is that by-productsfrom chlorine dioxide in the form of chlorate and chloriteions can have acute toxicological eVects (Bull et al. 1990).

Bromine

The biocidal activity of bromine, like chlorine, is due to theformation of a hypohalous acid in water, namely hypobro-mous acid (HOBr) (De Hayr et al. 1994). HOBr reacts withproteins in the microbial cells, disrupting essential metabo-lism (De Hayr et al. 1994). Dissociation of HOBr into itsrespective ions (H+ and OBr¡) reduces the biocidal activity,and this dissociation is driven by increasing pH (De Hayret al. 1994). However, unlike the hypochlorite ion, OBr¡

ions retain some biocidal activity (though less than HOBr)

(Anonymous 2007). Therefore, despite only 57% as HOBrat pH 8.5 (Pearch and OlliV (2005), cited in Anonymous2007), the solution remains eVective as a disinfestant. As aresult, the pH of the water to be treated is much less of anissue when using bromine compared to using chlorine.

There are numerous other advantages to using bromineover chlorine. Bromine is reported to have a broader rangeof eYcacy against a variety of pathogens and algae thanchlorine (Austin 1989), though there are few studies to sub-stantiate this claim. One example is a recent Australianstudy, where bromine at 0.5–30 mg/L was compared toother chemical disinfestants for its eYcacy to control Alter-naria, Botrytis, Colletotrichum, Cylindrocladium, Fusar-ium, and Rhizoctonia after 30 s to 30 min exposure(Anonymous 2007). Bromine provided complete control ofWve of the six fungi tested (with poor control of Alternaria)at the higher concentrations and longer durations of expo-sure, and reduced conidial concentrations at the lower andintermediate concentrations and exposure durations (Anon-ymous 2007). However, chlorine gave superior controlacross the fungi tested.

Like chlorine, bromine reacts readily with nitrogenouscompounds in water forming bromamine, but, unlike chlo-ramine, bromamine is comparable to free bromine as a dis-infectant (Johnson and Overby 1971; De Hayr et al. 1994;Yiasoumi et al. 2005; White 1999). Therefore in poor qual-ity irrigation water, to obtain a modest residual concentra-tion of free chlorine may require very high initialconcentrations of chlorine, while bromine could be used atmuch lower concentrations (Anonymous 2007). Also,while bromine, like chlorine, produces halogenated residu-als, which carry potential environmental and human healthhazards, the bromine residuals are generally less persistentthan those of chlorine (Anonymous 1998; De Hayr et al.1994; Stewart et al. 2001). Finally, bromine disinfestationcauses very little phytotoxicity, even at high applicationconcentrations of 100 ppm (Austin 1989).

Chlorine–bromine

In at least some applications, combining chlorine and bro-mine into a single disinfestation product can result in syner-gistic interactions for very eVective disinfestation(Cunningham and Taverner 2002). It has been reported thatchloro-bromination at 5–15 ppm is a comparable disinfes-tant to 50–100 ppm sodium hypochlorite (Cunningham andTaverner 2002). Yet this was not evident in a recent Austra-lian study, where bromine/chlorine at 0.5–30 mg/L wascompared to other chemical disinfestants for its eYcacy tocontrol Alternaria, Botrytis, Colletotrichum, Cylindrocla-dium, Fusarium, and Rhizoctonia after 30 s–30 min expo-sures (Anonymous 2007). Bromine/chlorine controlled fourof the six fungi tested (except Alternaria and Rhizoctonia)

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at the higher concentrations and longer durations of expo-sure and reduced conidial concentrations at the lower andintermediate concentrations and exposure durations (Anon-ymous 2007). However, chlorine gave superior controlacross the fungi tested.

In earlier work, chloro-bromination treatments eVec-tively controlled a range of fungal pathogens of cut Xowercrops and nursery plants (Mebalds et al. 1997b). Phytoph-thora cinnamomi chlamydospores were controlled in neu-tral (pH 6.5–7.0) dam water with a total chlorine/brominesolution of 2.9 ppm for 4 min, but required a concentrationof 8 ppm for 8 min for control in alkaline dam water (pH9.4). Pythium ultimum oospores were controlled after 8 mincontact time at 1.5 ppm total available chlorine/bromine indam water, and F. oxysporum spores were controlled aftersimilar doses. Alternaria alternata spores were the mostresistant with only 90% killed at 3.4 ppm total availablechlorine/bromine in dam water.

An advantage of chloro-bromination over chlorination asa disinfestation method for recycled irrigation water is thatit is more eVective than chlorine when disinfesting waterwith pH values above 7 (Anonymous 1997). The costs ofchloro-bromination systems vary but set-up and runningcosts are similar to chlorination (Anonymous 1997). Phyto-toxicity data are scarce but it is recommended that residualchlorine/bromine concentrations in irrigation water arebelow 1 ppm prior to application (Anonymous 1997). Highconcentrations of chlorine/bromine solutions may corrodesome metal Wttings (Anonymous 1997).

Iodine

In this system, recycled irrigation water is passed through aseries of iodine Wlters (Chin 2005). Iodine dosing is automatedand responsive to the organic load of the water (J. Franks,Ioteq, pers. comm.); and after treatment, iodine residues areremoved using an anion-exchange resin (Chin 2005). Theadvantages of this system are that it is safe [no chemicalmixing, automatic dosage adjustment, and shutdown ifrequired (J. Franks, Ioteq, pers. comm.)], has little potentialfor phytotoxicity, and is eVective in water with a broadrange of pH, EC levels, and organic loads (Chin 2005).However, it has high running costs and due to computer-based dosing, has the potential for technical breakdown anduser diYculty (Chin 2005).

While iodine killed propagules of the fungus F. oxyspo-rum f. sp. lycopersici at 0.7 ppm, it was not eVectiveagainst viruses, even at much greater concentrations (up to15 ppm) (Runia 1989, 1994a, 1995). One drawback of thissystem is that if carbon Wlters are used for the removal ofiodine residues, these also remove iron and copper leavingthe irrigation water deWcient in these nutrients (Runia1994a).

Ozone

Ozone is a strong oxidant, more than 1.5 times strongerthan chlorine and this gives the chemical its microbiocidalproperties by oxidizing and so disrupting cell membranes(Igura et al. 2004; Newman 2004). It has been reported tobe eYcacious against all pathogen types (Runia 1995;Yiasoumi et al. 2005), providing close to 100% mortality in4 min (Anonymous 1993). Igura et al. (2004) found thatozone inactivated F. oxysporum conidia in either sterilizedwater or inorganic soil-less nutrient medium (20£ strength)equally well over a range of temperatures, and that thehigher the initial ozone concentration, the more eVectivethe inactivation. MacDonald et al. (1997) found that ozonewas highly eYcacious at disinfesting irrigation wastewater,and it is probably best suited to moderate or low volumeirrigation systems. Rey et al. (2001) and Yamamoto et al.(1990) used ozone to successfully eliminate hyphae ofPythium spp. and three bacterial species, respectively, fromrecirculated nutrient solutions used in hydroponic culture.

Ozone treatments eVectively controlled a range of fungalpathogens of cut Xower crops and nursery plants (Mebaldset al. 1997b). Ozone controlled P. cinnamomi chlamydosp-ores at a dose of 0.6 ppm (initial dose of 1.2–2.4 ppm) for16 min. Pythium ultimum oospores were controlled with anozone dose of 1.2–1.5 ppm for 4 min in tap water and 0.4–0.7 ppm for 8 min in dam water. Fusarium oxysporumspores were controlled with an ozone dose of 1.75 ppm for4 min in dam water. Alternaria zinniae spores were moreresistant to ozone with only limited control with a dose of1.3 ppm for 16 min.

Besides being eYcacious against all plant pathogentypes, ozone also reacts with pesticides to decompose them,and so this is an added bonus if recycled water is contami-nated with phytotoxic levels of various pesticides (Runia1994a). Another advantage of ozone is its low environmen-tal hazard due to its very short half-life in water (<20 min)and its breakdown to oxygen and oxygenated by-products(Carruthers 1997; Ferraro 1998). Finally, it can provideadditional oxygen to the root system of plants, althoughhigh levels can be phytotoxic (Ferraro 1998). While thephytotoxic eVects of ozone gas are well known, the eVect ofaqueous ozone on plants may be less severe (Graham et al.2009) and may, in fact, be beneWcial to plants since lowdose ozone has been implicated in triggering systemicacquired resistance responses (Rao and Davis 2001;Graham et al. 2009; Pell et al. 1997). Graham et al. (2009)measured the growth parameters of Wve woody perennialnursery crops, after 6 weeks of overhead spray irrigationwith daily applications of water containing various levels ofaqueous ozone. Low residual ozone concentrations, suY-cient for pathogen control, did not cause any measurablenegative eVect on plant growth. Plant response to aqueous

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ozone will diVer with plant species and numerous other fac-tors, but this lack of phytotoxicity in at least some nurseryspecies, together with aqueous ozone having a short persis-tence period, is an advantage for the development of thistreatment method for the management of pathogens in recy-cled irrigation water (Graham et al. 2009).

One of the main disadvantages with an ozone disinfesta-tion system is that eYcacy is reduced in water with a highpH, high in organic matter, and high in nitrite, manganese,iron or bicarbonate concentrations (Mebalds et al. 1997a).This creates an ozone demand that leaves less ozone avail-able to act as a disinfectant (Runia 1994a). For iron, this isdependent on the type of iron chelate used (Vanachter et al.1988). When EDDHA [ethylenediamine-N,N�-bis(2-hydroxyphenylacetic acid)] is used, iron precipitates outand the eYcacy of ozone for disinfestation is greatlyreduced; when DTPA (diethylene triamine pentaaceticacid) or EDTA (ethylenediaminetetraacetic acid) are used,there is no substantial decrease in disinfestation eYcacy ofozone (Vanachter et al. 1988). Consequently, ozone is mosteVective in neutral to acidic water that is low in organicmatter (Anonymous 1997). Therefore, water should be pre-Wltered to decrease the load of organic compounds, treatedin batches in a closed tank where the pH is lowered by theaddition of acid, and ozone is injected simultaneously (vanOs 2000).

Other disadvantages include potential health and envi-ronmental hazards if ozone is not dissolved eYciently;gradual breakdown of plastic, brass, and rubber Wttings byoxidation; the need for expensive stainless steel and sili-cone Wttings; (Anonymous 1997; Mebalds et al. 1997a) andexpensive installation and maintenance costs for the safeproduction and delivery of ozone (Tu and Harwood 2005;Pettitt 2003; van Os and Alsanius 2004). Due to its instabil-ity, storage of ozone is not possible (Carruthers 1997). Con-sequently, it is generated on site by passing dry air (or pureoxygen, which is more costly) through an high energy elec-trical Weld, and using it immediately (Carruthers 1997; vanOs 2000; Anonymous 1993, 1997). The capital costs for theozone generator and inline monitor to measure the averagedose of ozone over time are quite expensive (Anonymous1997). Also any unused ozone must be extracted anddestroyed, usually via adsorption and reaction with granu-lated activated carbon, which (a) adds a cost since the car-bon must be renewed regularly and (b) cannot be used ifpure oxygen rather than air is the ozone source due to com-bustion potential (Carruthers 1997). Finally, initial ozonedose does not reXect Wnal ozone levels, not only due to theconcentrations of various components including iron, man-ganese, nitrite, ammonia, sulWdes and bicarbonate ions, andthe temperature and pH, but also due to non-linear ozonedecay (Newman 2004; Hoigné 1994; Mebalds et al. 1997b).This makes it diYcult for operators to accurately determine

the actual ozone dose applied to water and whether it isadequate for control of speciWc plant pathogens.

Hydrogen peroxide

Hydrogen peroxide is a strong oxidizer, but compared toozone, requires higher concentrations and longer exposuretimes to achieve the same disinfection (Runia 1995;Domingue et al. 1988). Concentrations of 1,000–3,000 ppmor an ORP of 750 mV have been suggested for the disinfec-tion of water (Newman 2004), though Ehret et al. (1999)reported that a much lower concentration of 200 ppm for24 h eVectively controlled Fusarium spores in recirculatednutrient solutions. EYcacy is improved by the addition ofactivators (Runia 1995) but is limited by high levels oforganic matter (Newman 2004). However, the treatment ofrecycled irrigation water with hydrogen peroxide haspotential environmental and occupational health and safetyhazards; residual hydrogen peroxide can have mutageniceVects (Bull et al. 1990); it has potential phytotoxic eVects;it causes gradual breakdown of plastic greenhouse struc-tures by oxidation; and the safe handling, delivery, andstorage of hydrogen peroxide can be diYcult and expensive(Tu and Harwood 2005).

One study combined the use of hydrogen peroxide withUV irradiation in UV-oxidation technology, by injectinghydrogen peroxide into recirculation water just prior toexposure to UV irradiation (Runia and Boonstra 2004). TheUV light breaks the bond between the oxygen atoms in thehydrogen peroxide, forming hydroxyl radicals, which arevery strong oxidizing agents. It is important to get the ini-tial concentration correct since excess hydrogen peroxideabsorbs UV light strongly and therefore competes with thepathogen being treated, and residual hydrogen peroxide inthe recirculation water can be phytotoxic (Runia and Boon-stra 2004). Particularly under low pH and high transmissionvalues of the recirculation water, this treatment methodlowered the energy input required, compared with UV irra-diation alone, for equivalent eYcacy of treating F. oxyspo-rum in recycled irrigation water.

Another study combined the use of hydrogen peroxidewith ozone, and achieved a reduction in the populations ofbacterial and fungal test species, removed pesticide (atra-zine) residues with 90% eYciency, while maintaining a sta-ble level of beneWcial bacteria (Langlais et al. 2001).

Surfactants

The addition of surfactants can kill Phytophthora species inrecycled irrigation water, preventing disease spread(Stanghellini et al. 2000, 1996; Yakabe and MacDonald2005; Yakabe 2007). Surfactants have been reported to lysethe plasma membrane and so only kill fungal structures that

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lack a cell wall, such as zoospores and vesicles of pythiaca-eous species such as Pythium, Phytophthora, and Olpidium(Stanghellini et al. 1996; Tomlinson and Thomas 1986).However, Yakabe and MacDonald (2005) and Yakabe(2007) reported that a surfactant derived from plant extractsand two cationic surfactants were lethal to mycelia and allforms of propagules of P. ramorum and also inhibited spo-rangia formation, zoospore formation, and zoospore motil-ity. The eYcacy of the surfactants was not impaired by thepresence of suspended solids, and they are generally non-corrosive, stable, non-phytotoxic, and less toxic to humans,compared to chlorine (Yakabe 2007). The eYcacy of sur-factants against other plant pathogens has not beenreported.

Acidic electrolyzed oxidizing (EO) water

Acidic electrolyzed oxidizing (EO) water, produced by elec-trolysis of deionized water containing a low concentration ofa salt, has a high oxidation–reduction potential (ORP), lowpH, contains hypochlorous acid, and displays strong fungi-cidal, bactericidal, and virucidal activity (Buck et al. 2002;Kim et al. 2000; Venkitanarayanan et al. 1999). The bacteri-cidal activity has been correlated with the concentration ofhypochlorous acid (Oomori et al. 2000; Nakagawara et al.1998) but is likely to be a combined eVect of free chlorine,low pH and high ORP (Venkitanarayanan et al. 1999). Bucket al. (2002) tested the in vitro fungicidal activity of EOwater against 22 fungal plant pathogenic species and foundthat EO water signiWcantly reduced or prevented the germi-nation of all species. Furthermore, EO water did not causeany phytotoxic symptoms on the foliage or Xowers of 22species of bedding plants (Buck et al. 2002, 2003), causingonly minor symptoms on Wve species. EO water producedby electrolysis of magnesium chloride was more phytotoxicthan that from potassium chloride or sodium chloride (Bucket al. 2003). Free chlorine measurements on the EO waterwere 54–71 ppm (Buck et al. 2002, 2003). Hong et al.(2003c) suggested EO water may have potential for disin-festing irrigation water. An added bonus is the claim that EOwater has potential as a plant growth stimulant (K. Mason,Envirolyte Australasia, pers. comm.).

Ionization

Ionizers (electro-oxidizers) can pass an electrical chargethrough recycled irrigation water to release copper andsilver ions from the anodes, which rupture the outer mem-brane of any resident microorganisms, causing death (Chin2005). While it is eVective against algae, certain bacteria(C. CliVord, Oz Aqua-Qld, pers. comm.) and Phytophthoraand Pythium, it has not been tested against a wide range ofpathogens (Chin 2005) but is so far ineVective against

Alternaria and Fusarium (C. CliVord, Oz Aqua-Qld, pers.comm.). Free copper and silver ions were ineVectiveagainst F. oxysporum and tobacco mosaic virus (TMV) inwaste water with a pH of 6.1 (Runia 1989), but the authorsuggested raising the pH above 7.5 to improve the eYcacy.The system is robust, simple to use, requires little mainte-nance, anodes last 1.5–6 years (C. CliVord, Oz Aqua-Qld,pers. comm.) and has a low capital cost (Chin 2005).

Antimicrobial compounds

Various chemicals have been evaluated for their antimicro-bial potential in numerous systems.

Peroxyacetic acid In water, peroxyacetic acid (PAA) dis-sociates into hydrogen peroxide and acetic acid (Pettitt2003). It is eVective at halting the spread of Phytophthoradisease in recycled irrigation water and has low phytotoxic-ity (Pettitt 2003). PAA has been used successfully in hot-water treatment of bulbs for controlling stem nematode andbasal rot caused by F. oxysporum f. sp. narcissi, causing100% mortality of spores (Hanks and LinWeld 1999). Hanksand LinWeld (1999) suggest that PAA would be an eVectivedisinfectant for many other plant pathogens. Further break-down of the hydrogen peroxide into oxygen and watermeans that this treatment method poses no environmentalor health hazards and, due to oxygen release, has additionalpotential as a growth stimulant (Flaherty 1995).

Nutrient amendment The addition of speciWc nutrients orthe creation of particular nutrient ratios in recycled irriga-tion water can aVect pathogens and interrupt infection andspread. The addition of calcium, as either calcium nitrate orcalcium chloride, can impede the production of zoosporesby Phytophthora parasitica and therefore limit infection(Schnitzler 2004; von Broembsen and Deacon 1997). Cal-cium suppressed zoospore release and motility and stimu-lated zoospore cysts to germinate in the absence of asuitable host (von Broembsen and Deacon 1997). The addi-tion of silicon reduced the occurrence of P. ultimum oncucumbers (Schnitzler 2004). A 4:1 potassium:nitrogenratio prevented disease caused by Erwinia carotovora ontomato (Schnitzler 2004). Care would need to be taken toensure that plant requirements were still being met.

CO2 CO2 holds promise as a method for killing zoosporesof P. nicotianae, a pathogen of many herbaceous and somewoody ornamental plants, that is often found in recycledirrigation water (Ahonsi et al. 2008, 2010). Bubbling CO2

through simulated recycled water infested with zoosporesat 110.4 mL (0.2 g)/min for 5 min consistently killed up to81% of zoospores, with only those that had encysted priorto treatment surviving.

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Fungicides Some producers, rather than controlling thepathogen in the water, instead control the resultant diseasethat it causes on the plants. Carlson et al. (2004) reportedthat fungicides are the control method most commonlyemployed for treating diseases caused by Pythium spp. inrecycled irrigation water. However, issues of fungicideresistance, expense and environmental pollution (Kuhajeket al. 2003; Sanders 1984; Sanders et al. 1985; GriYni et al.1999; Grech and Rijkenberg 1992; Moorman and Kim2004) make treating the source of the inoculum in alternateways more desirable.

A more targeted approach has been taken by Stringfel-low and Reddy (2005), who found that the systemic fungi-cide Agrifos (active ingredient: mono- and di-postassiumsalts of phosphorous acid) controlled Phytophthora speciesin recycled irrigation water and suggested injecting theproduct into irrigation systems as a potential disease controlstrategy. Similarly, Pettitt et al. (2008) examined theeYcacy of non-woven capillary matting fabric impregnatedwith a cupric hydroxide formulation as a barrier to themovement of infective Phytophthora zoospores in recycledirrigation systems. When the impregnated fabric was usedas production bed covers or disk inserts (disks covering theinner base of plant containers), it signiWcantly reduced dis-ease spread, evidenced by a reduction in incidence of symp-toms and infection of an hardy nursery stock species, and ofpropagule numbers determined using baiting and Wltration/selective plating assays (Pettitt et al. 2008). Most of thecopper remained bound to the fabric matting and did notaccumulate in the recycled irrigation water. Copper has alsobeen used by directly applying it to irrigation water for thecontrol of Phytophthora and Olpidium (Toppe and Thingg-aard 1998; Smith 1979). Other metals, such as zinc and sil-ver, have shown fungicidal promise, but their addition torecycled irrigation water presents potential phytotoxicityand environmental pollution issues (Vanachter et al. 1992,1993; Pettitt 2003; Tomlinson and Faithfull 1979).

Biological

Biological control agents

Disease suppressiveness can likely be enhanced by theaddition of speciWc amendments (Postma 2004). Amend-ment of recycled irrigation water with a speciWc nitrogenstabilizing chemical formulation selectively enhanced thepopulation of indigenous Xuorescent pseudomonads anddecreased disease caused by Phytophthora capsici on caps-icums and P. aphanidermatum on cucumber (Pagliacciaet al. 2004, 2007, 2008). The nitrogen stabilizing chemicalformulation selectively inhibited denitrifying bacteria,while the inert ingredients in the formulation acted as a car-bon source for other bacteria, namely Xuorescent pseudo-

monads, which, at a sustained threshold level, played a rolein disease suppression (Pagliaccia et al. 2007, 2008). Inaddition, the active ingredient in the formulation exhibitedin vitro fungicidal activity against Phytophthora and Pyth-ium zoospores (Pagliaccia et al. 2007, 2004). Also, thechemical formulation had a positive eVect on the growth ofcapsicum and gerbera plants and increased Xower produc-tion in gerberas (Pagliaccia et al. 2004).

The inundative addition of selected biological controlagents has been suggested to complement other treatmentmethods of limited eYcacy (Steinberg et al. 1994). Thesenon-pathogenic microorganisms could occupy the nichesleft by the pathogens removed by the treatment method,and proliferate, limiting growth, multiplication and so dis-ease potential of the surviving pathogens (Steinberg et al.1994). Pseudomonas Xuorescens had an antagonistic eVecton P. ultimum, and, in addition, a plant growth-promotiveeVect on the host tomato (Alsanius et al. 2004). Biologicalcontrol agents work by numerous mechanisms includingcompetition for space or nutrients, antibiosis, mycoparasit-ism, or induced resistance (Postma 2004). A recentlydescribed strategy of some biocontrol microorganisms isthe production of biosurfactants that rapidly lyse zoospores(Stanghellini and Miller 1997). The bacterium P. aerugin-osa produces biosurfactant rhamnolipids that can lyse zoo-spores of members of Phytophthora, Pythium, andPlasmopara (Stanghellini and Miller 1997), and so, may beuseful when added to recycled irrigation water for controlof diseases caused by these pathogens.

The suppressiveness of particular media in a productionsystem to certain plant pathogens can be helpful in limitingdisease. Strong et al. (1997) speculated that suppressive-ness was decreased when potting mix was steam pasteur-ized, leading to an increase in disease incidence andseverity caused by P. parasitica transmitted in recycledirrigation water in an ebb-and-Xow system. Similarly, sup-pressiveness of disease in cucumber caused by P. aphanid-ermatum was decreased in sterilized used rockwoolcompared to non-autoclaved used rockwool. Suppressive-ness only recovered after reinoculation with the originalmicroXora (Postma 2004; Postma et al. 2000). The use ofnon-sterilized rockwool may lead to other pest and diseaseissues; therefore, enhancing suppressiveness by introducingspeciWc microorganisms or products to stimulate growthand reproduction of suppressive microXora would be bene-Wcial (Postma et al. 2000).

The recirculating nutrient solutions of hydroponic sys-tems with a rock wool substrate have dense populations ofnon-pathogenic bacteria comprising various genera, whichmay have some value as biological control agents againstpathogenic microbes (Berkelmann et al. 1994). BeneWcialrhizobacteria present in recirculating nutrient solutions canreduce disease severity and yield loss caused by plant

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pathogens in such systems (Tu 2004). Tu et al. (1999)found that in a closed recirculating system, Pythium root rotwas less severe than in an open system, and this could beattributed to an increased rhizobacteria population in therecirculating solution.

The commercial application of biological control agentshas numerous challenges including target speciWcity, for-mulation, reWnement of the dose-reponse relationship, sta-bility, and reliability (Ehret et al. 2001).

BioWltration

A bioWlter contains a porous Wltering matrix, such as peat,rockwool, or scoria (lava grains) (Anonymous 2000),which support an active microbial population that areantagonistic to undesirable pathogens and break down vari-ous other contaminants such as heavy metals, nutrients, andphenolics, in water (Chin 2005). EYcacy of bioWltration isdue to the interaction between biological and physical fac-tors (Chin 2005) (so they cannot be classed exclusively as abiological method and inclusion in this section, as opposedto the section on physical methods, is somewhat arbitrary).BioWlters work with faster Xow rates than SSF, are safe andeasy to operate, and are simple and robust; however, theircapital cost is comparatively high (Chin 2005).

Some bioWlters contain a rotation system, which injectsair into the upper portion of the Wlter medium (Anonymous2000; Le Quillec et al. 2005). Upon addition of an inocu-lum of beneWcial bacteria (sometimes termed a biologicalactivator), the rotation system maximizes contact betweenthese beneWcial bacteria and the water to be treated, leadingto a rapid Wlter ripening time of only 24 h (Anonymous2000; Le Quillec et al. 2005). If being used in glasshouseproduction systems, it is recommended that the bioWltersystem is set up within the glasshouse (at 15–25°C) tomaintain optimal biological activity (Le Quillec et al.2005). It is also recommended that pesticides are not usedwithin the system to conserve the biological activity of theWlter (Le Quillec et al. 2005).

Constructed wetlands

Constructed wetlands may be either free-water surface wet-lands, where raw water Xows across and mostly above thesubstrate surface, or subsurface Xow wetlands, where rawwater Xows within the substrate and free water is not visible(Berghage et al. 1999; Hammer 1993). The latter may bemore appropriate for the treatment of greenhouse and nurs-ery eZuent, as it requires less land and minimizes expo-sure, which is desirable if the water contains pesticides andother contaminants (Berghage et al. 1999). A typical sub-surface Xow wetland is constructed of a lined basin Wlledwith a substrate, such as coarse gravel, that supports a

diverse microbial population and usually, higher plants(Berghage et al. 1999). Complex physical, chemical, andbiological interactions are involved between the raw water,the substrate, the microorganisms, and the higher plants(Berghage et al. 1999; Hammer 1993) to remove plantpathogens and other undesirable components such as pesti-cides and high nutrient levels (Arnold et al. 2004a; Fernan-dez et al. 1999; Holt et al. 1999; Lesikar et al. 1997).

The eYcacy of constructed wetlands to remove plantpathogens from nursery and greenhouse runoV water hasreceived little attention. In one study, after high concentra-tions of P. cinnamomi were seeded into inXuent of con-structed wetlands containing common reeds (Phragmitesaustralis), the pathogen was not detectable in the eZuent(Headley et al. 2005; Huett 2002). Even over a range ofseasons and after only short time periods within the wetland(as short as 1.3 days), the pathogen was unable to survivepassage through the wetland.

Constructed wetlands have advantages over other treat-ment methods in that they are relatively inexpensive, sim-ple to operate and require little maintenance. An addedbonus is that it can act as a propagation system for wetlandplant species, which are in demand for various reclamationprojects, providing an additional revenue source (Beagleand Justin 1993). Other ancillary beneWts include providingwildlife refuges, and recreational and environmental spaces(Hammer 1993). However, repeated recycling of waterthrough constructed wetlands may increase soluble salts tolevels that may be phytotoxic to nursery species (Arnoldet al. 2003, 2004b). Salt tolerance of nursery plants varieswith species, cultivar, climatic conditions, and irrigationmethod, with sub-canopy applications of irrigation waterrather than overhead application, reducing phytotoxicity(Arnold et al. 2003, 2004b; Niu and Rodriguez 2006a, b;Wu et al. 2001; Niu et al. 2007; Fox et al. 2005; Milbocker1988; Parnell 1988).

Other

Similar to constructed wetlands, ditch systems aredesigned to use multiple components to achieve Wltrationof recycled irrigation water and are separated into sec-tions on a series of interconnected levels (Jochems 2006).Water Xows from higher to lower levels over a weir,allowing aeration to maintain biological activity and max-imizing exposure to sunlight and the antimicrobial eVectof UV. Plants, such as irises and waterweeds, providehabitats for microbial populations with disease-suppres-sive characteristics, oxygenate the water, and removeexcess nutrients. Higher organisms, such as predatoryWsh, decrease population levels of plant pests, and snailsremove other sources of organic matter. Some nurseries inthe Netherlands have reported improved biodiversity, less

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Table 1 Advantages and disadvantages of common treatment methods employed to disinfest recycled irrigation water

Treatment method Advantages Disadvantages

Physical

Sedimentation (electro-coagulation)

SimpleSafe (no chemicals)Not aVected by variations in waterRemoves beneWcial microbes

Byproducts need to be removed regularly

Slow Wltration—sand SimpleSafe (no chemicals)Low tech, built/installed by laymenLow energyRetains natural microXoraNot aVected by variations in waterNo harmful residuals/byproductsNo preWlter requiredNo phytotoxicity

Large setup costToo slow for large quantities of waterFrequent clogging requires maintenanceLegionella bacteria part of microXoraOccasional eYcacy breakdownsSand is heavy—diYcult to construct/relocateGravel layers makes for large unit

Slow Wltration—rockwool SimpleSafe (no chemicals)Low techLow energyRetains natural microXoraNot aVected by variations in waterNo harmful residuals/byproductsLess dense than sand—easier

construction and relocationDoes not require gravel, smaller unitMuch less clogging, less maintenanceMore eYcacious with certain pathogensNo preWlter requiredNo phytotoxicity

Large setup costToo slow for large quantities of waterLegionella bacteria part of microXoraOccasional eYcacy breakdownsMore complex system than sand

Slow Wltration—pumice SimpleSafe (no chemicals)Low techLow energyRetains natural microXoraNot aVected by variations in waterNo harmful residuals/byproductsLess dense than sand—easier

construction and relocationHigher Wltration capacity, smaller unitMuch less clogging, less maintenanceMore eYcacious with certain pathogensNo preWlter requiredNo phytotoxicity

Large setup costToo slow for large quantities of waterLegionella bacteria part of microXoraOccasional eYcacy breakdownsMore complex system than sand

Membrane Highly eYcaciousSafe (no chemicals)AVected by solids in waterNot dependent on pHNo phytotoxicity

Probably not practical due to high costs, rapid cloggingPreWlter essential

Heat SimpleSafe (no chemicals)Low techNo harmful residuals/byproducts

ExpensiveNeed to cool water before applicationNeed to acidify water before treatmentKills beneWcial microbesCorrosiveWell tested in Europe

UV Non-corrosiveNot dependent on pHSafe (no chemicals)

AVected by solids in water > 60% transmissionPreWlter essentialLamp output decreases with age, so regular replacementPotential growth inhibition of plantsDestroys iron chelateNontarget eVects on beneWcial microbes

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Table 1 continued

Treatment method Advantages Disadvantages

Physical

Pressure SimpleSafe (no chemicals)Low techNo harmful residuals/byproductsNon-corrosive

Very little information availableMay only reduce inoculum not eliminate

Sonication Potential for selective controlSafe (no chemicals)No harmful residuals/byproductsNon-corrosive

Very little information availableIneYcient and uneconomicalHigh cooling requirementsSlow Xow ratesDelicate mechanism

Electrostatic precipitation

Safe (no chemicals) No information available

Chemical

Chlorine Stable residual to continue disinfestingCleans out algal and bacterial slimeHighly eYcaciousAs CaOCl, calcium is available for plant uptake

AVected by solids (esp. N) in waterAVected by pH of water, requires acidiWcationLong-lived byproducts with human

health and environmental hazardsPhytotoxicity if too high levelCorrosive(Chlorine gas unsafe)

Chlorine dioxide Broader pH range (cf. chlorine)Biocidal action not aVected by nitrogenous

compounds

Human health and environmental hazardsLack of phytotoxicity dataLack of eYcacy dataMust be produced and used onsite with

specialized equipment

Bromine Still eVective at higher pH (cf. chlorine)Broader range of pathogen eYcacyBiocidal action not aVected by nitrogenous

compoundsNot phytotoxic even at high levelsByproducts less persistent (cf. chlorine)

Byproducts with human health and environmental hazardsLack of eYcacy data

Chlorobromine Synergism improves eYcacy (reported)More eYcacious at higher pH (cf. chlorine)

Lack of phytotoxicity dataLack of eYcacy dataCorrosive

Iodine Dosing automatedSafe (no chemical mixing)Residues automatically removedNo phytotoxictyNot aVected by variations in water

Potential for technical breakdown and user diYculty

Ozone BeneWcial to plant growth (?)Degrades pesticidesLow environmental hazard

High capital costAVected by variations in waterPotential health hazardPotential phytotoxicityCorrosiveUnused ozone removed by carbon—adds costNo stable residualGenerated onsite, cannot be stored

Hydrogen peroxide SimpleLong history of use in food industry

Not as eYcacious as ozoneAVected by variations in waterPotential health and environmental hazardPhytotoxicCorrosiveSafe handling/delivery/storage diYcult, costly

Surfactants Not aVected by suspended solids in waterNo phytotoxicityNon-corrosiveFewer health hazards (cf. chlorine)Stable

Little information availableVery little use to date in nursery/greenhouseData only for pythiaceous species

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disease problems and have been able to signiWcantlyreduce fungicide use (Jochems 2006).

Integrated management and recommendations

All of the treatment methods available for disinfesting recy-cled irrigation water have advantages and disadvantages. Asummary of these for the main treatment methods is out-lined in Table 1. Integrated management of plant patho-gens, using a combination of cultural, physical, chemical,and biological methods, in nursery and greenhouse produc-

tion systems using recycled irrigation water, will be themost successful approach. For example, an 80% reductionin Pythium root rot of cucumber was achieved by Wrstlyacidifying the nutrient solution, then exposing it to UV irra-diation and Wnally, adding a bacterial bioagent (Tu 2004).

There is still much that is unknown when it comes totreating recycled irrigation water for resident plant patho-gens. Detailed information on the species diversity, lifecycle stage, and inoculum load of plant pathogens in recy-cled irrigation water is lacking. This information is requiredto ascertain the biological threshold for diVerent pathosys-tems, to aid in determining the economic injury level. Once

Table 1 continued

Treatment method Advantages Disadvantages

Chemical

EO water SimpleStable residual to continue disinfestingLess formation of harmful byproducts (cf. chlorine)No phytotoxicityNo health and environmental hazardEYcacious against plant pathogenic fungi,

other bacteria and virusesPotential plant growth stimulant

Lack of eYcacy data in waterLittle use to date in nursery/greenhouse

Ionization SimpleLittle maintenanceAnodes last years

Lack of eYcacy data

Peroxyacetic acid Low phytotoxicityNo health and environmental hazardPotential plant growth stimulant

Little information availableLack of eYcacy data

Nutrient amendment SimpleNon-corrosiveStable

Little information availableLimited eYcacy, only certain pathogensPotential phytotoxicity

CO2 Simple Little information availableLack of eYcacy dataNo use to date in nursery/greenhouse?

Fungicides Well studied Potential phytotoxicityPotential human and environmental hazardPotential resistanceExpensive

Biological

Biological control agents SpeciWc for target pathogen, reducing non-target eVects

Can be used to complement other treatmentsSome have plant growth promotion eVects

SpeciWcity may limit applicabilityLack of eYcacy data, especially adding to waterIssues with stability, reliability?

BioWlters SimpleSafe (no chemicals)Retains natural microXoraFaster Xow rates than slow WltrationRemoves nutrientsNo phytotoxicity

Need to replace nutrientsLittle use to date in nursery/greenhouse

Constructed wetlands SimpleSafe (no chemicals)Removes pesticides and nutrientsPropagation of wetland speciesLittle maintenance

Repeated recycling may increase soluble salts—phytotoxic

Need to replace nutrients

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economic thresholds are developed, this would enable pro-ducers to decide whether the expense of implementing adisinfestation program for particular pathogens is war-ranted. This would be done by regular testing of pathogenlevels in water and a case-by-case decision-making processas to the value of treatment application. Also, this informa-tion would enable assessment of the eYcacy of potentialdisinfestation treatments against realistic concentrations ofpropagules.

Further research is required to assess the eYcacy oftreatment technologies on important plant pathogens inrecycled irrigation water. There are many gaps in theknowledge [as an example, the Australian situation outlinedby Lane (2004)] and to enable producers to choose a disin-festation system that suits all their needs, this information isessential. Emerging treatment technologies for the nurseryand greenhouse industries need to be tested under actualuse conditions to ensure they are eYcacious and robust, andto assure producers of their applicability.

The development of national Best Practice Guidelinesfor each country for the speciWc treatment of individualplant pathogens in recycled irrigation water would ensurethat producers are clear about the best options for control-ling particular pathogens in their recycled irrigation water.Such a standardized approach would promote consistentquality management within the industry.

As our understanding of the ecology of the various plantpathogens in recycled irrigation water expands, so too doesour understanding of the best ways to eliminate or reducethem. With the need for recycling irrigation water escalat-ing, an holistic view of the problem combined with a Xexi-ble but focussed integrated management plan will providethe most sustainable solution.

Acknowledgments This review is based on a report of a study com-missioned by Nursery & Garden Industry Australia (NGIA) and fund-ed jointly by the Nursery Industry Levy and the CommonwealthGovernment via Horticulture Australia Limited (HAL) (Project #NY08002). The author thanks Dr Anthony Kachenko (NGIA) for con-structive comments on the draft manuscript of the original study report.

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