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14.2 Microorganisms in Aquaponics

5 months ago

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Microorganisms are present in the entire aquaponics system and play a key role in the system. They are consequently found in the fish, the filtration (mechanical and biological) and the crop parts. Commonly, the characterisation of microbiota (i.e. microorganisms of a particular environment) is carried out on circulating water, periphyton, plants (rhizosphere, phyllosphere and fruit surface), biofilter, fish feed, fish gut and fish faeces. Up until now, in aquaponics, most of microbial research has focused on nitrifying bacteria (Schmautz et al. 2017). Thus, the trend at present is to characterise microorganisms in all compartments of the system using modern sequencing technologies. Schmautz et al. (2017) identified the microbial composition in different parts of the system, whereas Munguia-Fragozo et al. (2015) give perspectives on how to characterize aquaponics microbiota from a taxonomical and functional point of view by using cutting-edge technologies. In the following sub-sections, focus will be only brought on microorganisms interacting with plants in aquaponic systems organised into plant beneficial and plant pathogenic microorganisms.

14.2.1 Plant Pathogens

Plant pathogens occurring in aquaponic systems are theoretically those commonly found in soilless systems. A specificity of aquaponic and hydroponic plant culture is the continuous presence of water in the system. This humid/aquatic environment suits almost every plant pathogenic fungus or bacteria. For root pathogens some are particularly well adapted to these conditions like pseudo-fungi belonging to the taxa of Oomycetes (e.g. root rot diseases caused by Pythium spp. and Phytophthora spp.) which are able to produce a motile form of dissemination called zoospores. These zoospores are able to move actively in liquid water and thus are able to spread over the entire system extremely quickly. Once a plant is infected, the disease can rapidly spread out the system, especially because of the water's recirculation (Jarvis 1992; Hong and Moorman 2005; Sutton et al. 2006; Postma et al. 2008; Vallance et al. 2010; Rakocy 2012; Rosberg 2014; Somerville et al. 2014). Though Oomycetes are among the most prevalent pathogens detected during root diseases, they often form a complex with other pathogens. Some Fusarium species (with existence of species well adapted to aquatic environment) or species from the genera Colletotrichum, Rhizoctonia and Thielaviopsis can be found as part of these complexes and can also cause significant damage on their own (Paulitz and Bélanger 2001; Hong and Moorman 2005; Postma et al. 2008; Vallance et al. 2010). Other fungal genera like Verticillium and Didymella, but also bacteria, such as Ralstonia, Xanthomonas, Clavibacter, Erwinia and Pseudomonas, as well as viruses (e.g. tomato mosaic, cucumber mosaic, melon necrotic spot virus, lettuce infectious virus and tobacco necrosis), can be detected in hydroponics or irrigation water and cause vessel, stem, leaf or fruit damage (Jarvis 1992; Hong and Moorman 2005). However note that not all microorganisms detected are damaging or lead to symptoms in the crop. Even species of the same genus can be either harmful or beneficial (e.g. Fusarium, Phoma, Pseudomonas). Disease agents discussed above are mainly pathogens linked to water recirculation but can be identified in greenhouses also. Section 14.2.2 shows the results of the first international survey on plant diseases occurring specifically in aquaponics, while Jarvis (1992) and Albajes et al. (2002) give a broader view of occurring pathogens in greenhouse structures.

In hydroponics or in aquaponic systems, plants generally grow under greenhouse conditions optimized for plant production, especially for large-scale production where all the environmental parameters are computer managed (Albajes et al. 2002; Vallance et al. 2010; Somerville et al. 2014; Parvatha Reddy 2016). However, optimal conditions for plant production can also be exploited by plant pathogens. In fact, these structures generate warm, humid, windless and rain-free conditions that can encourage plant diseases if they are not correctly managed (ibid.). To counteract this, compromises must be made between optimal plant conditions and disease prevention (ibid.). In the microclimate of the greenhouse, an inappropriate management of the vapour-pressure deficit can lead to the formation of a film or a drop of water on the plants surface. This often promotes plant pathogen development. Moreover, to maximise the yield in commercial hydroponics, some other parameters (e.g. high plant density, high fertilisation, to extend the period production) can enhance the susceptibility of plants to develop diseases (ibid.).

The question now is to know by which route the initial inoculum (i.e. the first step in an epidemiological cycle) is brought into the system. The different steps in plant disease epidemiological cycle (EpC) are represented in Fig. 14.1. In aquaponics, as in greenhouse hydroponic culture, it can be considered that entry of pathogens could be linked to water supply, introduction of infected plants or seeds, the growth material (e.g. reuse of the media), air exchange (dust and particles carriage), insects (vectors of diseases and particles carriage) and staff (tools and clothing) (Paulitz and Bélanger 2001; Albajes et al. 2002; Hong and Moorman 2005; Sutton et al. 2006; Parvatha Reddy 2016).

img src="https://cdn.aquaponics.ai/thumbnails/2a6cd3eb-6917-49d2-97ba-36e508ee48b0.jpg" style="zoom:50%;" /

Fig. 14.1 Basic steps (1 to 6) in plant disease epidemiological cycle (EpC) according to Lepoivre (2003). (1) Arrival of the pathogen inoculum, (2) contact with the host plant, (3) tissues penetration and infection process by the pathogen, (4) symptoms development, (5) plant tissues that become infectious, (6) release and spread of infectious form of dispersion

Once the inoculum is in contact with the plant (step 2 in the EpC), several cases of infection (step 3 in the EpC) are possible (Lepoivre 2003):

  • The pathogen-plant relationship is incompatible (non-host relation) and disease does not develop.

  • There is a host relation but the plant does not show symptoms (the plant is tolerant).

  • The pathogen and the plant are compatible but defence response is strong enough to inhibit the progression of the disease (the plant is resistant: interaction between host resistance gene and pathogen avirulence gene).

  • The plant is sensitive (host relation without gene for gene recognition), and the pathogen infects the plant, but symptoms are not highly severe (step 4 in the EpC).

  • And lastly, the plant is sensitive and disease symptoms are visible and severe (step 4 in the EpC).

Regardless of the degree of resistance, some environmental conditions or factors can influence the susceptibility of a plant to be infected, either by a weakening of the plant or by promoting the growth of the plant pathogen (Colhoun 1973; Jarvis 1992; Cherif et al. 1997; Alhussaen 2006; Somerville et al. 2014). The main environmental factors influencing plant pathogens and disease development are temperature, relative humidity (RH) and light (ibid.). In hydroponics, temperature and oxygen concentrations within the nutrient solution can constitute additional factors (Cherif et al. 1997; Alhussaen 2006; Somerville et al. 2014). Each pathogen has its own preference of environmental conditions which can vary during its epidemiologic cycle. But in a general way, high humidity and temperature are favourable to the accomplishment of key steps in the pathogen's epidemic cycle such as spore production or spore germination (Fig. 14.1, step 5 in the EpC) (Colhoun 1973; Jarvis 1992; Cherif et al. 1997; Alhussaen 2006; Somerville et al. 2014). Colhoun (1973) sums up the effects of the various factors promoting plant diseases in soil, whereas Table 14.1 shows the more specific or adding factors that may encourage plant pathogen development linked to aquaponic greenhouse conditions.

In the epidemiological cycle, once the infective stage is reached (step 5 in the EpC), the pathogens can spread in several ways (Fig. 14.1, step 6 in the EpC) and infect other plants. As explained before, root pathogens belonging to Oomycetes taxa can actively spread in the recirculating water by zoospores release (Alhussaen 2006; Sutton et al. 2006). For other fungi, bacteria and viruses responsible for root or aerial diseases, the dispersion of the causal agent can occur by propagation of infected material, mechanical wounds, infected tools, vectors (e.g. insects) and particles (e.g. spores and propagules) ejection or carriage allowed by drought, draughts or water splashes (Albajes et al. 2002; Lepoivre 2003).

14.2.2 Survey on Aquaponic Plant Diseases

During January 2018, the first international survey on plant diseases was made among aquaponics practitioner members of the COST FA1305, the American Aquaponics Association and the EU Aquaponics Hub. Twenty-eight answers were

Table 14.1 Adding factors encouraging plant pathogen development under aquaponic greenhouse structure compared to classical greenhouse culture

table thead tr class="header" thPromoting factor/th th Profiting to /th th Causes /th th References /th /tr /thead tbody tr class="odd" tdNutrient film technique (NFT), Deep flow technique (DFT)/td td iPythium/i spp., iFusarium/i spp. /td td Easy spread by water recirculation; possibility of post contamination after a disinfection step; poor content in oxygen in the nutrient solution /td td Koohakan et al. (2004) and Vallance et al. (2010) /td /tr tr class="even" tdInorganic media (e.g. rockwool)/td td Higher content in bacteria (no information about their possible pathogenicity) /td td Unavailable organic compounds in the media /td td Khalil and Alsanius (2001), Koohakan et al. (2004), Vallance et al. (2010) /td /tr tr class="odd" tdOrganic media (e.g. coconut fibre and peat)/td td Higher content in fungi; higher content in Fusarium spp. for coconut fibre /td td Available organic compounds in the media /td td Koohakan et al. (2004), Khalil et al. (2009), and Vallance et al. (2010) /td /tr tr class="even" tdMedia with high water content and low content in oxygen (e.g. rockwool)/td td iPythium/i spp. /td td Zoospores mobility; plant stress /td td Van Der Gaag and Wever (2005), Vallance et al. (2010), and Khalil and Alsanius (2011) /td /tr tr class="odd" tdMedia allowing little water movement (e.g. rockwool)/td td iPythium/i spp. /td td Better condition for zoospores dispersal and chemotaxis movement; no loss of zoospore flagella /td td Sutton et al. (2006) /td /tr tr class="even" tdHigh temperature and low concentration of DO in the nutrient solution/td td iPythium/i spp. /td td Plant stressed and optimal condition for iPythium/i growth /td td Cherif et al. (1997), Sutton et al. (2006), Vallance et al. (2010), and Rosberg (2014) /td /tr tr class="odd" tdHigh host plant density and resulting microclimate/td td Pathogens growth; diseases spread /td td Warm and humid environment /td td Albajes et al. (2002) and Somerville et al. (2014) /td /tr tr class="even" tdDeficiencies, excess or imbalance of macro/ micronutrients/td td Fungi, viruses and bacteria /td td Plant physiological modifications (e.g. action on defence response, transpiration, integrity of cell walls); plant morphological modifications (e.g. higher susceptibility to pathogens, attraction of pests); nutrient resources in host tissues for pathogens; direct action on the pathogen development cycle /td td Colhoun (1973), Snoeijers and Alejandro (2000), Mitchell et al. (2003), Dordas (2008), Veresoglou et al. (2013), Somerville et al. (2014), and Geary et al. (2015) /td /tr /tbody /table

received describing 32 aquaponic systems from around the world (EU, 21; North America, 5; South America, 1; Africa, 4; Asia, 1). The first finding was the small response rate. Among the possible explanations for the reluctance to reply to the questionnaire was that practitioners did not feel able to communicate about plant pathogens because of a lack of knowledge on this topic. This had already been observed in the surveys of Love et al. (2015) and Villarroel et al. (2016). Key information obtained from the survey are:

  • 84.4% of practitioners observe disease in their system.

  • 78.1% cannot identify the causal agent of a disease.

  • 34.4% do not apply disease control measures.

  • 34.4% use physical or chemical water treatment.

  • 6.2% use pesticides or biopesticides in coupled aquaponic system against plant pathogens.

These results support the previous arguments saying that aquaponic plants do get diseases. Yet, practitioners suffer from a lack of knowledge about plant pathogens and disease control measures actually used are essentially based on non-curative actions (90.5% of cases).

In the survey, a listing of plant pathogens occurring in their aquaponic system was provided. Table 14.2 shows the results of this identification. To remedy the lack of practitioner's expertise about plant disease diagnostics, a second survey version was

Table 14.2 Results of the first identifications of plant pathogens in aquaponics from the 2018 international survey analysis and from existing literature

table thead tr class="header" thPlant host/th th Plant pathogen /th th References or survey results /th /tr /thead tbody tr class="odd" tdAllium schoenoprasu/td td Pythium sp.sup(b)/sup /td td Survey /td /tr tr class="even" tdBeta vulgaris (swiss chard)/td td Erysiphe betaesup(a)/sup /td td Survey /td /tr tr class="odd" tdCucumis sativus/td td Podosphaera xanthiisup(a)/sup /td td Survey /td /tr tr class="even" tdFragaria spp./td td Botrytis cinereasup(a)/sup /td td Survey /td /tr tr class="odd" tdLactuca sativa/td td Botrytis cinereasup(a)/sup /td td Survey /td /tr tr class="even" td/td td Bremia lactucaesup(a)/sup /td td Survey /td /tr tr class="odd" td/td td Fusarium sp.sup(b)/sup /td td Survey /td /tr tr class="even" td/td td Pythium dissotocumsup(b)/sup /td td Rakocy (2012) /td /tr tr class="odd" td/td td Pythium myriotylumsup(b)/sup /td td Rakocy (2012) /td /tr tr class="even" td/td td Sclerotinia sp.sup(a)/sup /td td Survey /td /tr tr class="odd" tdMentha spp./td td Pythium sp.sup(b)/sup /td td Survey /td /tr tr class="even" tdNasturtium officinale/td td Aspergillus sp.sup(a)/sup /td td Survey /td /tr tr class="odd" tdOcimum basilicum/td td Alternaria sp.sup(a)/sup /td td Survey /td /tr tr class="even" td/td td Botrytis cinereasup(a)/sup /td td Survey /td /tr tr class="odd" td/td td Pythium sp.sup(b)/sup /td td Survey /td /tr tr class="even" td/td td Sclerotinia sp.sup(a)/sup /td td Survey /td /tr tr class="odd" tdPisum sativum/td td Erysiphe pisisup(a)/sup /td td Survey /td /tr tr class="even" tdSolanum lycopersicum/td td Pseudomononas solanacearumsup(a)/sup /td td McMurty et al. (1990) /td /tr tr class="odd" td/td td Phytophthora infestanssup(a)/sup /td td Survey /td /tr /tbody /table

Plant pathogens identified by symptoms in the aerial plant part are annotated by (a) and in root part by (b) in exponent sent with the aim to identify symptoms without disease name linkage (Table 14.3). Table 14.2 mainly identifies diseases with specific symptoms, i.e. symptoms that can be directly linked to a plant pathogen. It is the case of Botrytis cinerea and its typical grey mould, powdery mildew (Erysiphe and Podosphaera genera in the table) and its white powdery mycelium/conidia, and lastly Sclerotinia spp. and its sclerotia production. The presence of 3 plant pathologists in the survey respondents expands the list, with the identification of some root pathogens (e.g. Pythium spp.). General symptoms that are not specific enough to be directly related to a pathogen without further verification (see diagnosis in Sect. 14.3) are consequently found in Table 14.3. But it is important to highlight that most of the symptoms observed in this table could also be the consequence of abiotic stresses. Foliar chlorosis is one of the most explicit examples because it can be related to a large number of pathogens (e.g. for lettuces: Pythium spp., Bremia lactucae, Sclerotinia spp., beet western yellows virus), to environmental conditions (e.g. temperature excess) and to mineral deficiencies (nitrogen, magnesium, potassium, calcium, sulfur, iron, copper, boron, zinc, molybdenum) (Lepoivre 2003; Resh 2013).

Table 14.3 Review of occurring symptoms in aquaponics from the 2018 international survey analysis

table thead tr class="header" thSymptoms/th th Plants species /th /tr /thead tbody tr class="odd" tdFoliar chlorosis/td td Allium schoenoprasum sup1/sup, Amaranthus viridis sup1/sup, Coriandrum sativum sup1/sup, iCucumis sativus/i sup1/sup, iOcimum basilicum/i sup6/sup, iLactuca sativa/i sup4/sup, Mentha spp. sup2/sup, iPetroselinum crispum/i sup1/sup, Spinacia oleracea sup2/sup, iSolanum lycopersicum/i sup1/sup, Fragaria spp. sup1/sup /td /tr tr class="even" tdFoliar necrosis/td td Mentha spp. sup2/sup, iOcimum basilicum/i sup1/sup, /td /tr tr class="odd" tdStem necrosis/td td iSolanum lycopersicum/i sup1/sup, /td /tr tr class="even" tdCollar necrosis/td td iOcimum basilicum/i sup1/sup /td /tr tr class="odd" tdFoliar Mosaic/td td iCucumis sativus/i sup1/sup, Mentha spp. sup1/sup, iOcimum basilicum/i sup1/sup, /td /tr tr class="even" tdFoliar wilting/td td Brassica oleracea Acephala group sup1/sup, iLactuca sativa/i sup1/sup, Mentha spp. sup1/sup, iCucumis sativus/i sup1/sup, iOcimum basilicum/i sup1/sup, iSolanum lycopersicum/i sup1/sup /td /tr tr class="odd" tdFoliar, stem and collar mould/td td Allium schoenoprasum sup1/sup, iCapsicum annuum/i sup1/sup, iCucumis sativus/i sup1/sup, iLactuca sativa/i sup2/sup, Mentha spp. sup2/sup, iOcimum basilicum/i sup4/sup, iSolanum lycopersicum/i sup1/sup /td /tr tr class="even" tdFoliar spots/td td iCapsicum annuum/i sup1/sup, iCucumis sativus/i sup1/sup, iLactuca sativa/i sup2/sup, Mentha spp. sup1/sup, iOcimum basilicum/i sup5/sup /td /tr tr class="odd" tdDamping off/td td Spinacia oleracea sup1/sup, iOcimum basilicum/i sup1/sup, iSolanum lycopersicum/i sup1/sup, seedlings in general sup5/sup /td /tr tr class="even" tdCrinkle/td td iBeta vulgaris/i (swiss chard) sup1/sup, iCapsicum annuum/i sup1/sup, iLactuca sativa/i sup1/sup, iOcimum basilicum/i sup1/sup /td /tr tr class="odd" tdBrowning or decaying root/td td Allium schoenoprasum sup1/sup, Amaranthus viridis sup1/sup, iBeta vulgaris/i (swiss chard) sup1/sup, Coriandrum sativum sup1/sup, iLactuca sativa/i sup1/sup, Mentha spp. sup2/sup, iOcimum basilicum/i sup2/sup, iPetroselinum crispum/i sup2/sup, iSolanum lycopersicum/i sup1/sup, Spinacia oleracea sup1/sup /td /tr /tbody /table

Numbers in exponent represent the occurrence of the symptom for a specific plant on a total of 32 aquaponic systems reviewed

14.2.3 Beneficial Microorganisms in Aquaponics: The Possibilities

As explained in the introduction, several publications focused on bacteria involved in the nitrogen cycle, while others already emphasise the potential presence of beneficial microorganisms interacting with plant pathogens and/or plants (Rakocy 2012; Gravel et al. 2015; Sirakov et al. 2016). This section reviews the potential of plant beneficial microorganisms involved in aquaponics and their modes of action.

Sirakov et al. (2016) screened antagonistic bacteria against Pythium ultimum isolated from an aquaponic system. Among the 964 tested isolates, 86 showed a strong inhibitory effect on Pythium ultimum in vitro. Further research must be achieved to taxonomically identify these bacteria and evaluate their potential in in vivo conditions. The authors assume that many of these isolates belong to the genus Pseudomonas. Schmautz et al. (2017) came to the same conclusion by identifying Pseudomonas spp. in the rhizosphere of lettuce. Antagonistic species of the genus Pseudomonas were able to control plant pathogens in natural environments (e.g. in suppressive soils) while this action is also affected by environmental conditions. They can protect plants against pathogens either in an active or a passive way by eliciting a plant defence response, playing a role in plant growth promotion, compete with pathogens for space and nutrients (e.g. iron competition by release of iron-chelating siderophores), and/or finally by production of antibiotics or antifungal metabolites such as biosurfactants (Arras and Arru 1997; Ganeshan and Kumar 2005; Haas and Défago 2005; Beneduzi et al. 2012; Narayanasamy 2013). Although no identification of microorganisms was done by Gravel et al. (2015)), they report that fish effluents have the capacity to stimulate plant growth, decrease the mycelial growth of Pythium ultimum and Pythium oxysporum in vitro and reduce the colonization of tomato root by these fungi.

Information about the possible natural plant protection capacity of aquaponic microbiota is scarce, but the potential of this protective action can be envisaged with regard to different elements already known in hydroponics or in recirculated aquaculture. A first study was conducted in 1995 on suppressive action or suppressiveness promoted by microorganisms in soilless culture (McPherson et al. 1995). Suppressiveness in hydroponics, here defined by Postma et al. (2008)), has been "referred to the cases where (i) the pathogen does not establish or persist; or (ii) establishes but causes little or no damage". The suppressive action of a milieu can be related to the abiotic environment (e.g. pH and organic matter). However, in most situations, it is considered to be related directly or indirectly to microorganisms' activity or their metabolites (James and Becker 2007). In soilless culture, the suppressive capacity shown by water solution or the soilless media is reviewed by Postma et al. (2008) and Vallance et al. (2010). In these reviews, microorganisms responsible for this suppressive action are not clearly identified. In contrast, plant pathogens like Phytophthora cryptogea, Pythium spp., Pythium aphanidermatum and Fusarium oxysporum f.sp. radicis-lycopersici controlled or suppressed by the natural microbiota are exhaustively described. In the various articles reviewed by Postma et al. (2008) and Vallance et al. (2010), microbial involvement in the suppressive effect is generally verified via a destruction of the microbiota of the soilless substrate by sterilisation first and eventually followed by a re-inoculation. When compared with an open system without recirculation, suppressive activity in soilless systems could be explained by the water recirculation (McPherson et al. 1995; Tu et al. 1999, cited by Postma et al. 2008) which could allow a better development and spread of beneficial microorganisms (Vallance et al. 2010).

Since 2010, suppressiveness of hydroponic systems has been generally accepted and research topics have been more driven on isolation and characterization of antagonistic strains in soilless culture with Pseudomonas species as main organisms studied. If it was demonstrated that soilless culture systems can offer suppressive capacity, there is no similar demonstration of such activity in aquaponics systems. However, there is no empiric indication that it should not be the case. This optimism arises from the discoveries of Gravel et al. (2015) and Sirakov et al. (2016) described in the second paragraph of this section. Moreover, it has been shown in hydroponics (Haarhoff and Cleasby 1991 cited by Calvo-bado et al. 2003; Van Os et al. 1999) but also in water treatment for human consumption (reviewed by Verma et al. 2017) that slow filtration (described in Sect. 14.3.1) and more precisely slow sand filtration can also act against plant pathogens by a microbial suppressive action in addition to other physical factors. In hydroponics, slow filtration has been demonstrated to be effective against the plant pathogens reviewed in Table 14.4. It is assumed that the microbial suppressive activity in the filters is most probably due to species of Bacillus and/or Pseudomonas (Brand 2001; Déniel et al. 2004; Renault et al. 2007; Renault et al. 2012). The results of Déniel et al. (2004) suggest that in hydroponics, the mode of action of Pseudomonas and Bacillus relies on competition for nutrients and antibiosis, respectively. However, additional modes of action could be present for these two genera as already explained for Pseudomonas spp. Bacillus species can, depending on the environment, act either indirectly by plant biostimulation or elicitation of plant defences or directly by antagonism via production of antifungal and/or antibacterial substances. Cell wall-degrading enzymes, bacteriocins, and antibiotics, lipopeptides (i.e. biosurfactants), are identified as key molecules for the latter action (Pérez-García et al. 2011; Beneduzi et al. 2012; Narayanasamy 2013). All things considered, the functioning of a slow filter is not so different from the functioning of some biofilters used in aquaponics. Furthermore, some heterotrophic bacteria like Pseudomonas spp. were already identified in aquaponics biofilters (Schmautz et al. 2017). This is in accordance with the results of other researchers who frequently detected Bacillus and/or Pseudomonas in RAS (recirculated aquaculture system) biofilters (Tal et al. 2003; Sugita et al. 2005; Schreier et al. 2010; Munguia-Fragozo et al. 2015; Rurangwa and Verdegem 2015). Nevertheless, up until now, no study about the possible suppressiveness in aquaponic biofilters has been carried out.

Table 14.4 Review of plant pathogens effectively removed by slow filtration in hydroponics

table thead tr class="header" thPlant pathogens/th th References /th /tr /thead tbody tr class="odd" tdiXanthomonas campestris/i pv. iPelargonii/i/td td Brand (2001) /td /tr tr class="even" tdiFusarium oxysporum/i/td td Wohanka (1995), Ehret et al. (1999) cited by Ehret et al. (2001), van Os et al. (2001), Déniel et al. (2004), and Furtner et al. (2007) /td /tr tr class="odd" tdiPythium/i spp./td td Déniel et al. (2004) /td /tr tr class="even" tdiPythium aphanidermatum/i/td td Ehret et al. (1999) cited by Ehret et al. (2001), and Furtner et al. (2007) /td /tr tr class="odd" tdiPhytophthora cinnamomi/i/td td Van Os et al. (1999), 4 references cited by Ehret et al. (2001) /td /tr tr class="even" tdiPhytophthora cryptogea/i/td td Calvo-bado et al. (2003) /td /tr tr class="odd" tdiPhytophthora cactorum/i/td td Evenhuis et al. (2014) /td /tr /tbody /table