Venturia inaequalis (apple scab)
Identity
- Preferred Scientific Name
- Venturia inaequalis (Cooke) G.Winter
- Preferred Common Name
- apple scab
- Other Scientific Names
- Endostigme inaequalis (Cooke) Syd.
- Fusicladium pomi (Fr.) Lind
- Helminthosporium pirinum Lib. (pro parte)
- Sphaerella cinerascens Fuckel
- Sphaerella inaequalis Cooke
- Sphaeria cinerascens Fuckel
- Spilocaea pomi Fr.
- Spilosticta inaequalis (Cooke) Petr.
- International Common Names
- Englishblack spot: applescab: apple
- Spanishmoteado del manzanorona del manzanosarna del manzano
- Frenchtacontavelure du pommiertavelure du sorbier
- Local Common Names
- GermanyLagerschorf: ApfelSchorf: Apfel
- EPPO code
- VENTIN (Venturia inaequalis)
Pictures
Distribution
Host Plants and Other Plants Affected
Host | Host status | References |
---|---|---|
Cotoneaster | Other | |
Crataegus laevigata | Other | |
Malus (ornamental species apple) | Other | |
Malus baccata (siberian crab apple) | Other | |
Malus domestica (apple) | Main | Ebrahimi and Fotouhifar (2015) Stehmann et al. (2001) Charest et al. (2002) McKirdy et al. (2001) Martínez-Bilbao and Murillo (2005) Holb et al. (2005) |
Malus floribunda | Other | |
Pyracantha (Firethorn) | Other | |
Pyrus (pears) | Other | |
Pyrus communis (European pear) | Other | |
Sorbus (rowan) | Other | |
Viburnum | Other |
Symptoms
V. inaequalis has been widely studied (Oberhofer, 1985; Gupta, 1992; MacHardy, 1996; Agrios, 1997b; Biggs, 1997). MacHardy (1996) provides a historical survey on all aspects of V. inaequalis. Apple scab attacks leaves, petioles, blossoms, sepals, fruits, pedicels and less frequently, young shoots and bud scales. The most obvious symptoms can be observed on leaves and fruits. The first infection in spring can occur on sepals in the phenological stage of 'bud break'. They are the first green organs exposed to infections and are an important source of secondary inoculum for developing fruits (Kennel, 1987).As the leaves emerge in spring, the undersides, in particular the surface adjacent to the midrib, is the first and most exposed surface. Infection on expanding leaves generally leads to large scab lesions, which distort the leaves. Infection of unfolded leaves, where the upper surface of the leaves is more exposed, usually results in smaller lesions due to an increase in natural resistance (Schwabe, 1979; Sanogo and Aylor, 1997).Young scab spots appear as a light shade of green, which contrasts slighty with the healthy leaf surface. The lesions soon become olive-green to grey with a velvety surface due to the abundant production of conidiophores and conidia. Later, some lesions appear metallic black (black spot) and may be slightly raised. The number of lesions per leaf may range from one or two to several hundred. Lesions resulting from ascospore infection remain more distinct, while secondary infections by conidia lead to spots, which may coalesce. The term 'sheet scab' is often used to classify leaves that are entirely covered with scab. Defoliation occurs when the leaves are heavily attacked (MacHardy, 1996).Lesions on young fruit appear similar to those on leaves, but they usually enlarge more slowly, become darker in colour and are more sharply bordered. The lesions progress to bare, brown and corky spots. Fruit infections early in the season can affect meristematic tissue and, because of this, regeneration by callus is stopped after such injuries. When the fruits enlarge, cracks appear in the skin and the fruit flesh, but often early infected fruits drop prematurely. An apple becomes more resistant during development (Schwabe et al., 1984). Fruits infected when approaching maturity form only small lesions, and these may not be visible until the apples are in storage. These circular, black lesions, ranging from 0.1 to 4 mm in diameter, have been referred to as 'pin-point' or 'pin-head scab'.Occasionally scab lesions are produced on bud scales, which can be an important source of conidial inoculum in spring. Such scab pustules may also appear on apple twigs but are more commonly caused by Venturia pirina on pear; in Germany this is described as 'grindschorf'. Wood scab on apple is most often observed in poorly managed orchards. A special form of scab on apple shoots was first observed in Germany by Kennel (Moosherr, 1990; Moosherr and Kennel, 1995) and is referred as 'superficial shoot scab'.
List of Symptoms/Signs
Symptom or sign | Life stages | Sign or diagnosis |
---|---|---|
Plants/Fruit/abnormal shape | ||
Plants/Fruit/lesions: scab or pitting | ||
Plants/Inflorescence/blight; necrosis | ||
Plants/Leaves/fungal growth | ||
Plants/Leaves/necrotic areas |
Prevention and Control
Host-Plant Resistance
Breeding programmes are in progress to develop high-quality apple cultivars that are resistant to V. inaequalis (Fischer et al., 1998; Kellerhals et al., 1997, 1998; Goerre et al., 1999; Lateur et al., 1999). In the past, such programmes have mainly been based on the monogenic resistance from Malus floribunda 821 (Vf). In 1988, at Ahrensburg, Germany, small sporulating scab lesions were found on some Vf -hybrid selections. It was later found in other countries that this resistance was not of a durable type. Different races of apple scab are already detected (Kruger et al., 1999). The appearance of race 6, overcoming the resistance of cultivars with the Vf gene and race 7, overcoming the resistance in Malus floribunda (Benaouf and Parisi, 2000) has lead to new breeding programmes with the aim to develop cultivars with a different genetic basis for resistance against scab. Genetically controlled resistance exists for at least five genes (Vf, Vm, Vr, Vb and Vbj) (Hemmat et al., 2000).
DARE (Durable Apple Resistance in Europe), set up in 1998 as a joint project between different institutes in Europe was an important initiative to develop durable resistance in new apple varieties to scab and powdery mildew (Lespinasse et al., 2000).
Investigations on the virulence pattern in field isolates of V. inaequalis provided evidence that variation between isolates depends on the biodiversity within the planted cultivars. Orchards with few or only one main cultivar selected a more homogeneous scab population, with all isolates carrying the specific virulence to the dominant cultivar. This offers opportunities to reduce the susceptibility, depending of the planting design of an orchard. In a mixed orchard a large share of the pathogen population will be eliminated from the epidemic process in spring as the ascospores will land on tissue of a non-host (Koch et al., 2000).
Genetic studies suggest that in addition to short distance gene flow, dispersal over longer distance by humans also occurs, probably due to transport of infected plant material (Tenzer and Gessler, 1999).
Molecular biological techniques on varieties and scab strains can improve the search on which varieties should be planted together to enhance the biodiversity in an orchard and to reduce the spread of apple scab in such orchards (MacHardy et al., 2001).
Polygenic resistance and gene transfer technology is the basis for obtaining more tolerant cultivars (Rees et al., 1996; Kellerhals et al., 1997; Lespinasse et al., 1999; Aldwinckle et al., 1999).
Conventional breeding of scab-resistant apple varieties requires at least 15 years. Resistance in these varieties is based on a single gene, which is not very durable, and the quality of most resistant varieties on the market today is below that which would be accepted by the consumer. Multiple resistance genes are desirable but this is very difficult to realize using conventional methods. Researchers around the world are involved in the development and optimisation of protocols for transformation of different apple cultivars of high market value. Different transgenes, encoding for antifungal proteins with activity against apple scab are already isolated (Broothaerts et al., 2000; Norelli et al., 2000; Chevreau et al., 2001; Bolar et al., 2001).
The aim of omitting all fungicide treatments against scab is no longer relevant. A few fungicide applications, based on infection risk during the primary season, may be necessary for durable control in the future. Genetic resistance should be a valid complement to the use of fungicides rather than an alternative.
Sanitation
A low primary inoculum orchard is a major requirement for successful scab control. Measurements that accelerate the rate of leaf decomposition can strongly reduce the scab inoculum in the orchard (MacHardy, 2000). Overwintering inoculum can be reduced by leaf shredding, or by the application of urea just prior to leaf fall or to the leaves on the ground (Gupta, 1992; Cimanowski et al., 1997; Heijne et al., 2000). Urea applied to the leaf litter in November reduced the number of ascospores trapped by 50% (Sutton et al., 2000). Urea acts directly on scab and it increases leaf nitrogen, which stimulates microorganisms to break down the leaves more rapidly. However, applications with high doses of urea may have negative secondary effects on the tree. Late nitrogen application could give a growing stimulus, which may result in serious damage of the flower buds at early night frost (Wood et al., 2000). Moreover, extra nitrogen uptake in the wood may makes the leaf scars more sensitive to canker infections, caused by Nectria galligena (Creemers, 1996b). With leaf shredding, the scab infestation was reduced in the next year by 88, 82 and 75%, respectively, on sepals, rosette and shoot leaves (Creemers and Vanmechelen, 2001).
A new sanitation technique 'Sweep&Vacuum' is now being investigated by W. MacHardy. This technique involves sweeping and vacuuming the leaves, with the aim of removing 90% or more of the leaf litter from the orchard floor.
The leaf fall period is the most critical period for fruit tree canker infection through the leaf scars. The most efficient fungicides for control are the benzimidazoles and the copper syntheses, but both groups are harmful to the activity of earthworms, the most important organisms for leaf decomposition and soil airing in a perennial culture system (Aalbers, 2001). Such compounds are no longer recommended in orchards with scab problems. Imazalil is a possible alternative fungicide for canker control. Positive results were obtained using imazalil applied during leaf fall in combination with trisiloxane based surfactants.
Desilets et al. (1997) reported on the potential of propane flamers for the reduction of primary inoculum on the orchard floor.
Cultural Control
Trees should be planted in the orchard in such a way that aeration after rainfall or dew leads to rapid drying of susceptible tissues in the tree canopy. Trees should be pruned regularly, to enhance drying and improve spray coverage. However, orchards with vigorously growing trees, resulting from heavy pruning or regrowth after early summer pruning, are especially susceptible to late scab infections and to the overwintering of scab mycelium or conidia on the tree (Triloff, 1994).
The use of growth regulators can also reduce the risk of scab. Recently, the growth regulator prohexadione-calcium was registered in different countries. It was estimated that four anti-scab treatments could be saved if growth was stopped 6 weeks earlier than normal (Deckers and Daemen, 2000).
Biological Control
Two fungi may be potentially useful as biological control agents against V. inaequalis (Miedtke and Kennel, 1990). Athelia bombacina (Fiaccadori and Cesari, 1998), applied just prior to leaf fall, is especially effective in suppressing the production of ascospores and to a lesser extent in stimulating leaf decomposition by softening the leaves. Chaetomium globosum applied during the secondary scab season is beneficial in reducing the spread of scab.
Carisse and co-workers (Philion et al., 1997; Carisse et al., 1999, 2000; Carisse and Dewdney, 2002) recently investigated antagonistic fungi showing potential to reducing the production of pseudothecia. Promising results in reducing ascospore production were obtained with a species of Microsphaeropsis, strain P130A.
Isolation and characterization of epiphytic fungi and bacteria from the phyllosphere of apple offers possibilities to select potential biocontrol agents against scab in its biotrophic phase (Fiss et al., 2000).
Infection Models
A number of fungicides are at the disposal of the fruit grower for control of apple scab. In regions with favourable weather conditions for scab infection, 70% or more of the total amount of pesticides applied are used against this disease. The move towards the adoption of monocultures of a single apple variety, and the ban of the use of plant growth regulators to shorten the growth period and infection period, has increased the infection pressure to such a level that one mistake in the spray programme can lead to economic disaster. In such circumstances, fungicides with a higher performance are indispensable.
In contrast, the consumer is more concerned with the environmental effects of pesticides and residues on fruits. The introduction of IPM is essential for the survival of fruit production. For IPM, the control of fungal diseases is mainly based on the reduction of the inoculum in the orchard, the determination of the infection risks during the growing season and the use of selective fungicides that do not harm beneficial organisms. From a calendar spray scheme using more or less fixed spraying intervals, there has been an evolution towards treatments that are based on warning devices. These warning systems have become increasingly more electronic, which has facilitated the transfer of meteorological data to a central point for the calculation of the infection risks in different regions. The integration of biological factors such as orchard inoculum, ascospore release and leaf growth can give a better estimation of the real scab risk in a favourable climatological period for scab (Kohl et al., 1994; Manktelow et al., 1997; Kollar, 1997; Creemers et al., 1998). Several simulation models are in development as alternatives to the laborious work needed for the determination of these biological parameters: Rimpro (Trapman and Polfliet, 1997), Welte (Welte, 1999), Clean Arbo (Huberdeau and Geoffrion, 1998; Baudry and Orts, 1999), Adem (Berrie, 1997; Xu and Butt, 1997) and Spraycheck (Stewart et al., 1998).
More details of these models can be found on the following websites:
http://www.biofruitadvies.nl (RIMpro)
http://www.farmsoft.de/index.html (Schorfprognose)
http://www.hri.ac.uk/site2/research/fres.htm (Adem)
http://www.ctifl.fr (Clean Arbo)
Other methods which facilitate the forecast of ascospore release in the orchard are described by Berkett (1996), Tshmir and Kolesova (1996) and Kollar (Kollar, 1998).
Warning systems are currently based exclusively on a curative approach but in future it would be useful to take into account the weather forecast (Villalta et al., 2002). Calculation of leaf wetness, as done for the Aschorf model developed by KP Wittich (Friesland and Wittich, 2002) at the German weather Service (http://agromet-cost.istea.bo.cnr.it/aschorf.pdf) may provide an opportunity for a more practical approach for local warning services (Creemers, 2001).
The strategy to change to a preventive warning service based on weather forecast offers different practical advantages:
· Better timing of application in relation to spray conditions (soil and weather conditions)
· Reduced selection pressure for resistance to curative fungicides, while more preventive fungicides are used in the spray schedule
· Holistic approach of pest and diseases with less spray events
· Spray technique and especially spray coverage is more important for curative than for preventive treatments
· Better planning and organization of labour on the farm
· Only preventive fungicides available in organic farming
The use of new high performance fungicides is only one aspect of the control strategy. Different fungicide families must be applied during the growing season in relation to optimal biological and climatological conditions. The combined use of different types of fungicides with complementary effects and a limited number of treatments with one fungicide type used per season will prolong the lifetime of newly developed fungicide groups. Anti-resistance strategies in the spray schedule for modern fungicides is a challenge for the control of diseases that require several treatments in one season.
Breeding programmes are in progress to develop high-quality apple cultivars that are resistant to V. inaequalis (Fischer et al., 1998; Kellerhals et al., 1997, 1998; Goerre et al., 1999; Lateur et al., 1999). In the past, such programmes have mainly been based on the monogenic resistance from Malus floribunda 821 (Vf). In 1988, at Ahrensburg, Germany, small sporulating scab lesions were found on some Vf -hybrid selections. It was later found in other countries that this resistance was not of a durable type. Different races of apple scab are already detected (Kruger et al., 1999). The appearance of race 6, overcoming the resistance of cultivars with the Vf gene and race 7, overcoming the resistance in Malus floribunda (Benaouf and Parisi, 2000) has lead to new breeding programmes with the aim to develop cultivars with a different genetic basis for resistance against scab. Genetically controlled resistance exists for at least five genes (Vf, Vm, Vr, Vb and Vbj) (Hemmat et al., 2000).
DARE (Durable Apple Resistance in Europe), set up in 1998 as a joint project between different institutes in Europe was an important initiative to develop durable resistance in new apple varieties to scab and powdery mildew (Lespinasse et al., 2000).
Investigations on the virulence pattern in field isolates of V. inaequalis provided evidence that variation between isolates depends on the biodiversity within the planted cultivars. Orchards with few or only one main cultivar selected a more homogeneous scab population, with all isolates carrying the specific virulence to the dominant cultivar. This offers opportunities to reduce the susceptibility, depending of the planting design of an orchard. In a mixed orchard a large share of the pathogen population will be eliminated from the epidemic process in spring as the ascospores will land on tissue of a non-host (Koch et al., 2000).
Genetic studies suggest that in addition to short distance gene flow, dispersal over longer distance by humans also occurs, probably due to transport of infected plant material (Tenzer and Gessler, 1999).
Molecular biological techniques on varieties and scab strains can improve the search on which varieties should be planted together to enhance the biodiversity in an orchard and to reduce the spread of apple scab in such orchards (MacHardy et al., 2001).
Polygenic resistance and gene transfer technology is the basis for obtaining more tolerant cultivars (Rees et al., 1996; Kellerhals et al., 1997; Lespinasse et al., 1999; Aldwinckle et al., 1999).
Conventional breeding of scab-resistant apple varieties requires at least 15 years. Resistance in these varieties is based on a single gene, which is not very durable, and the quality of most resistant varieties on the market today is below that which would be accepted by the consumer. Multiple resistance genes are desirable but this is very difficult to realize using conventional methods. Researchers around the world are involved in the development and optimisation of protocols for transformation of different apple cultivars of high market value. Different transgenes, encoding for antifungal proteins with activity against apple scab are already isolated (Broothaerts et al., 2000; Norelli et al., 2000; Chevreau et al., 2001; Bolar et al., 2001).
The aim of omitting all fungicide treatments against scab is no longer relevant. A few fungicide applications, based on infection risk during the primary season, may be necessary for durable control in the future. Genetic resistance should be a valid complement to the use of fungicides rather than an alternative.
Sanitation
A low primary inoculum orchard is a major requirement for successful scab control. Measurements that accelerate the rate of leaf decomposition can strongly reduce the scab inoculum in the orchard (MacHardy, 2000). Overwintering inoculum can be reduced by leaf shredding, or by the application of urea just prior to leaf fall or to the leaves on the ground (Gupta, 1992; Cimanowski et al., 1997; Heijne et al., 2000). Urea applied to the leaf litter in November reduced the number of ascospores trapped by 50% (Sutton et al., 2000). Urea acts directly on scab and it increases leaf nitrogen, which stimulates microorganisms to break down the leaves more rapidly. However, applications with high doses of urea may have negative secondary effects on the tree. Late nitrogen application could give a growing stimulus, which may result in serious damage of the flower buds at early night frost (Wood et al., 2000). Moreover, extra nitrogen uptake in the wood may makes the leaf scars more sensitive to canker infections, caused by Nectria galligena (Creemers, 1996b). With leaf shredding, the scab infestation was reduced in the next year by 88, 82 and 75%, respectively, on sepals, rosette and shoot leaves (Creemers and Vanmechelen, 2001).
A new sanitation technique 'Sweep&Vacuum' is now being investigated by W. MacHardy. This technique involves sweeping and vacuuming the leaves, with the aim of removing 90% or more of the leaf litter from the orchard floor.
The leaf fall period is the most critical period for fruit tree canker infection through the leaf scars. The most efficient fungicides for control are the benzimidazoles and the copper syntheses, but both groups are harmful to the activity of earthworms, the most important organisms for leaf decomposition and soil airing in a perennial culture system (Aalbers, 2001). Such compounds are no longer recommended in orchards with scab problems. Imazalil is a possible alternative fungicide for canker control. Positive results were obtained using imazalil applied during leaf fall in combination with trisiloxane based surfactants.
Desilets et al. (1997) reported on the potential of propane flamers for the reduction of primary inoculum on the orchard floor.
Cultural Control
Trees should be planted in the orchard in such a way that aeration after rainfall or dew leads to rapid drying of susceptible tissues in the tree canopy. Trees should be pruned regularly, to enhance drying and improve spray coverage. However, orchards with vigorously growing trees, resulting from heavy pruning or regrowth after early summer pruning, are especially susceptible to late scab infections and to the overwintering of scab mycelium or conidia on the tree (Triloff, 1994).
The use of growth regulators can also reduce the risk of scab. Recently, the growth regulator prohexadione-calcium was registered in different countries. It was estimated that four anti-scab treatments could be saved if growth was stopped 6 weeks earlier than normal (Deckers and Daemen, 2000).
Biological Control
Two fungi may be potentially useful as biological control agents against V. inaequalis (Miedtke and Kennel, 1990). Athelia bombacina (Fiaccadori and Cesari, 1998), applied just prior to leaf fall, is especially effective in suppressing the production of ascospores and to a lesser extent in stimulating leaf decomposition by softening the leaves. Chaetomium globosum applied during the secondary scab season is beneficial in reducing the spread of scab.
Carisse and co-workers (Philion et al., 1997; Carisse et al., 1999, 2000; Carisse and Dewdney, 2002) recently investigated antagonistic fungi showing potential to reducing the production of pseudothecia. Promising results in reducing ascospore production were obtained with a species of Microsphaeropsis, strain P130A.
Isolation and characterization of epiphytic fungi and bacteria from the phyllosphere of apple offers possibilities to select potential biocontrol agents against scab in its biotrophic phase (Fiss et al., 2000).
Infection Models
A number of fungicides are at the disposal of the fruit grower for control of apple scab. In regions with favourable weather conditions for scab infection, 70% or more of the total amount of pesticides applied are used against this disease. The move towards the adoption of monocultures of a single apple variety, and the ban of the use of plant growth regulators to shorten the growth period and infection period, has increased the infection pressure to such a level that one mistake in the spray programme can lead to economic disaster. In such circumstances, fungicides with a higher performance are indispensable.
In contrast, the consumer is more concerned with the environmental effects of pesticides and residues on fruits. The introduction of IPM is essential for the survival of fruit production. For IPM, the control of fungal diseases is mainly based on the reduction of the inoculum in the orchard, the determination of the infection risks during the growing season and the use of selective fungicides that do not harm beneficial organisms. From a calendar spray scheme using more or less fixed spraying intervals, there has been an evolution towards treatments that are based on warning devices. These warning systems have become increasingly more electronic, which has facilitated the transfer of meteorological data to a central point for the calculation of the infection risks in different regions. The integration of biological factors such as orchard inoculum, ascospore release and leaf growth can give a better estimation of the real scab risk in a favourable climatological period for scab (Kohl et al., 1994; Manktelow et al., 1997; Kollar, 1997; Creemers et al., 1998). Several simulation models are in development as alternatives to the laborious work needed for the determination of these biological parameters: Rimpro (Trapman and Polfliet, 1997), Welte (Welte, 1999), Clean Arbo (Huberdeau and Geoffrion, 1998; Baudry and Orts, 1999), Adem (Berrie, 1997; Xu and Butt, 1997) and Spraycheck (Stewart et al., 1998).
More details of these models can be found on the following websites:
http://www.biofruitadvies.nl (RIMpro)
http://www.farmsoft.de/index.html (Schorfprognose)
http://www.hri.ac.uk/site2/research/fres.htm (Adem)
http://www.ctifl.fr (Clean Arbo)
Other methods which facilitate the forecast of ascospore release in the orchard are described by Berkett (1996), Tshmir and Kolesova (1996) and Kollar (Kollar, 1998).
Warning systems are currently based exclusively on a curative approach but in future it would be useful to take into account the weather forecast (Villalta et al., 2002). Calculation of leaf wetness, as done for the Aschorf model developed by KP Wittich (Friesland and Wittich, 2002) at the German weather Service (http://agromet-cost.istea.bo.cnr.it/aschorf.pdf) may provide an opportunity for a more practical approach for local warning services (Creemers, 2001).
The strategy to change to a preventive warning service based on weather forecast offers different practical advantages:
· Better timing of application in relation to spray conditions (soil and weather conditions)
· Reduced selection pressure for resistance to curative fungicides, while more preventive fungicides are used in the spray schedule
· Holistic approach of pest and diseases with less spray events
· Spray technique and especially spray coverage is more important for curative than for preventive treatments
· Better planning and organization of labour on the farm
· Only preventive fungicides available in organic farming
The use of new high performance fungicides is only one aspect of the control strategy. Different fungicide families must be applied during the growing season in relation to optimal biological and climatological conditions. The combined use of different types of fungicides with complementary effects and a limited number of treatments with one fungicide type used per season will prolong the lifetime of newly developed fungicide groups. Anti-resistance strategies in the spray schedule for modern fungicides is a challenge for the control of diseases that require several treatments in one season.
Chemical Control
Due to the variable regulations around (de-)registration of pesticides, we are for the moment not including any specific chemical control recommendations. For further information, we recommend you visit the following resources:
•
EU pesticides database (http://ec.europa.eu/food/plant/pesticides/eu-pesticides-database/)
•
PAN pesticide database (www.pesticideinfo.org)
•
Your national pesticide guide
Impact
Losses from scab over a period of years far exceed those from any other disease or pest of apples. The major economic loss to the grower is the reduction in fruit quality of scabbed apples. Severe attack of the leaves will cause mid-season defoliation and a reduction of tree vigour which, in turn may led to failure of fruit bud formation and to stunted and reduced growth. In regions and years with favourable weather conditions for scab infection and with a high PAD, nearly all the fruits may be infected. In such regions, about 70% of the pesticides applied are used in relation to scab control.
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Published online: 16 November 2021
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