5.1. Diseases of Black Pepper: Indian Institute of Spices Research, Kozhikode-673 012, Kerala, India

5.1.
DISEASES OF BLACK PEPPER

M.ANANDARAJ
Indian Institute of Spices Research, Kozhikode-673 012, Kerala,

India
Black pepper is affected by several diseases caused by fungi, bacteria, virus and
mycoplasma, besides nutritional disorders. Crop losses due to diseases and pests are
identified as major causes of low productivity of pepper in India (Sarma and
Anandaraj 1997). The earliest record of diseases of pepper in India was that of Barber
(1903, 1905). Butler (1906) also recorded the death of pepper and Rao (1929)
isolated Phytophthora from diseased pepper, but the etiology remained
inconclusive. Ridley (1912) referred to three important diseases of pepper namely,
canker, hyphae in vessels and wilt. The cause of wilt was not confirmed but assumed
to be due to fungi such as Nectria, Cephalosporium and Fusarium. Menon (1949),
while reviewing the diseases of pepper, reported that stump rot was due to Rosellinia
bunodes, “pollu” disease caused by Colletotrichum sp. and root disease or wilt due
to an unknown pathogen. From the diseased plants Nectria sp. was recorded, but
pathogenicity was not proved. Crop losses caused by diseases are a major production
constraints in all pepper producing countries. In Brazil root rot and stem blight
caused by Fusarium solani f. sp. piperis and the mosaic disease caused by cucumber
mosaic virus are the major diseases (Duarte and Albuquerque 1991), whereas, in
India, Indonesia and Malaysia Phytophthora foot rot is the major disease (Sarma et al
1992c, Holliday and Mowat 1963, Kueh and Sim 1992d, Manohara et al. 1992).
Other diseases include slow decline, anthracnose, viral diseases which are referred to
as stunted disease (Sarma et al. 1991), stunted growth (Sitepu and Kasim 1991) and
wrinkled leaf disease (Kueh and Sim 1992b). In India, although wilt disease was the
major disease causing death of plants, Phytophthora as the causal organism was
reported only in 1966 by Samraj and Jose. Several diseases were recorded
subsequently and now 17 diseases are known to affect pepper (Sarma et al. 1991).The
diseases of pepper are reviewed recently (Sarma et al. 1991, 1994, Anandaraj and
Sarma 1995). Among these diseases, Phytophthora foot rot, slow decline which were
previously referred to as “quick wilt” and “slow wilt” respectively (Nambiar and
Sarma 1977, Nambiar 1978, Das and Cheeran 1986), anthracnose and stunted disease
cause severe crop losses. Phytophthora capsici occur both in the nursery as well as in
the main field affecting all parts of the plant while others are confined to specific
plant parts. Based on the severity of crop losses caused, pepper diseases are classified
into major and minor diseases. The major diseases are treated here with greater
details.
239
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Harwood Academic Publishers imprint, part of The Gordon and Breach Publishing Group.
240 M.ANANDARAJ
MAJOR DISEASES
Phytopbthora Diseases in Pepper

Phytophthora capsici occurs on all parts of the plant and cause severe economic
damage. The symptom expression depends upon site of infection and extent of
damage (Mammootty 1978, Anandaraj and Sarma 1995). Phytophthora infections in
pepper is broadly classified into aerial and soil infections. Aerial infection occurs on
the runner shoots, foliage, spikes and branches causing blight, spike shedding,
defoliation and die back and at times death of plants. Infection on the runner shoots
often reach the collar causing foot rot.
Symptoms of foliar infection

On leaves one to many dark spots having characteristic fimbriate advancing margins
occur, which later coalesce leading to defoliation even before the lesions spread to
the entire lamina. Infections on runner shoots (stolons) that arise at the base of the
vines and trail on the ground occur both on the tender leaves and shoots. The fungus
sporulates abundantly forming a white covering on the blighted tender shoot.
Infection on tender shoots upon reaching the stem, cause, collar infection and sudden
wilting of plant. Infection on spikes causes blackening of developing fruits and
peduncle. Infection can start on any part of the spike and in due course affected
spikes are shed. Infection on branches causes drying and defoliation (Fig. 5.1.1). In
Brazil, Fusarium infection on pepper is severe and occur both on stem and root.
Infection of root results in destruction of feeder roots leading to flaccidity, yellowing
and defoliation. Stem infection results in yellowing and blighting of stem and
complete death of plants (Duarte and Albuquerque 1991).
Symptoms on roots and collar

Infection on below ground parts such as roots and collar is fatal. Infections of feeder
roots causes their rotting and degeneration resulting in yellowing, defoliation and
drying up of plants. Feeder root infection reaches the collar through main roots and
causes foot rot (Anandaraj et al. 1994). Pepper being vegetatively propagated, roots
arise at each node of the main stem which remain below the soil. If the infection reaches
the collar, either through the runner shoots or through the roots closer to the soil level,
plants show only wilting symptoms, whereas, infection reaching the collar through
roots of the lower nodes leads to yellowing and defoliation before succumbing to the
infection. Such plants may remain alive for 2–3 years (Anandaraj 1997).
Etiology of Phytophthora foot rot

Foot rot results in sudden wilting and death of plants and hence the disease was
previously referred to as either “quick wilt” or “wilt’, and the causal organism was
DISEASES 241
Figure 5.1.1 Symptoms due to Phytophthora capsici infection on black pepper

a. A wilting pepper vine due to collar rot
b. Infection of upper tier of roots culminating in collar rot
c. Infection on spikes
d. Foliar yellowing caused by root rot
e. Infection on feeder roots spreading to main roots and collar
f. Leaf spot showing fimbriate margins at the advancing edge of lesion
242 M.ANANDARAJ
identified as Phytophthora palmivora var piperis (Samraj and Jose 1966), P.

palmivora (Holliday and Mowat 1963, Manmohandas and Abicheeran 1985,
Nambiar 1978, Nambiar and Sarma 1977, Sarma and Nambiar 1982, Sarma et al.
1982, Nambiar et al. 1978), P. palmivora MF4 (Ramachandran et al. 1986, Sastry
1982, Sastry and Hegde 1982a, 1982b, 1987a, 1987b, 1991). Foot rot resulting from
root infection takes a longer time to kill the affected plants and they remain in the
field showing declining symptoms. A method to index the level of infection based on
foliar symptoms has been developed (Abraham et al. 1996).
Identity of the pathogen

Phytophthora isolates from infected pepper plants when cultured on carrot agar,
incubated for 72 h in dark followed by incubation of culture discs of 1 cm in Petri’s
mineral solution under fluorescent light for 24 h lead to abundant sporulation. The
sporangial ontogeny is umbellate with caducous sporangia. Sporangia are borne on
long stalks which were ellipsoidal with tapering base, obvoid or fusiform and with a
clear papilla. The mean L×B is 24.6×16.34 µm, the L×B ratio 2.0–2.05 in 58.5 per
cent of sporangia and 1.5–1.8 in the remaining. Based on the sporangial characters,
the isolates from foot rot affected pepper plantations are identified as Phytophthora
palmivora MF4 (Sarma et al. 1982, Tsao et al. 1985, Tsao and Alizadeh 1988,
Manohara and Sato 1992). In Johore region of Malaysia, P. parasitica var nicotianae
and P. botryosa are reported to cause sudden wilt of pepper (Varughese and Anuar
1992).
Isolation from soil

P. palmivora MF4 from pepper can be isolated from soil and plant tissues using
selective media. Among the selective media tried, PVPH medium (Tsao and Guy
1977) is found to be the best. Direct isolation from soil is not successful always, but,
pepper leaf (Kueh and Khew 1982) or pepper leaf discs (Ramachandran et al. 1986)
are good baits. The fungus could be isolated by using castor seeds as baits (Sastry and
Hegde 1987a, 1987b). Albizia falcataria leaflets when used as baits, the fungus
sporulate on the baits facilitating confirmation of positive baiting by direct
observation of infected baits and this could be brought into pure culture by plating
on selective medium (Anandaraj and Sarma 1990). This technique is also adopted for
assaying chemicals applied to soil to control Phytophthora foot rot (Anandaraj and
Sarma 1991).
Biology of the pathogen

Growth was studied on potato dextrose agar (PDA), cornmeal agar and oats agar. The
effect of temperature on the growth of the fungus was studied at 10°C–35°C. Growth
was least at 10°C (6 mm) and abundant at 24°C (46 mm) after 72 h and there was no
growth at 35°C. Pepper isolates are heterothallic and oospores are produced when
DISEASES 243
pepper isolates are paired with isolates from cocoa and rubber (Sarma and Nambiar
1982). Oospores are produced when compatible types are inoculated on pepper and
incubated in dark at 20°C and also in the presence of Trichoderma viride but,
oospores are not produced at 30°C (Brasier 1969, 1978). The production of toxin was
studied by culturing the fungus in Bartnicki-Garcia’s liquid medium (Ribeiro 1978).
Cell free culture filtrate from pepper isolates are reported to cause vascular browning
and flaccidity of leaves in bioassay (Sarma and Nambiar 1982).
Taxonomy of pepper Phytophthora

The foot rot pathogen of pepper Phytophthora, has been referred to as P. palmivora in
the literature (Holliday and Mowat 1963, Kueh 1979, Nambiar and Sarma 1977,
Sarma and Nambiar 1982). As the isolates are different from the typical P. palmivora,
it was called as an atypical P. palmivora (Waterhouse 1974), and was named P.
palmivora MF 4 in the revised tabular key by Stamps et al. (1990). Most
Phytophthora isolates from pepper have an umbellate sporangial ontogeny with
long caducous sporangia resembling that of P. capsici (Tsao et al. 1985). After
detailed morphological and biochemical studies, P. palmivora MF4 was merged with
P. capsici as most isolates from pepper resembled P. capsici. The species was
redescribed (Tsao and Alizadeh 1988, Tsao 1991) and is currently named P. capsici.
Phytophthora isolates from pepper from Indonesia belong to both A1 and A2 mating
types (Kasim and Prayitno 1979, Manohara and Sato 1992, Bandra et al. 1985). In
India, during the International Pepper Community Workshop in Goa, it was decided
to refer this disease as Phytophthora foot rot and the organism as P. capsici (Nair and
Sarma 1988). Since then extensive biochemical studies of P. capsici collected from
all over the world have revealed the presence of three electrophoretic types Cap1,
Cap2 and Cap3 (Oudemans and Coffey 1991). Based on analysis of 113 isolates of P.
capsici for morphological, physiological and isozyme data for 18 loci for 15
enzymes, two sub groups CapA and CapB were recognized. Indian isolates from
pepper have been reported to belong to both sub groups (Mchau and Coffey 1995).
Holliday (1998) in his Dictionary of Plant Pathology (2nd edition) designated it as P.
capsici f. sp. piperis, as this only attacks Piper and therefore differs from the f. sp.
capsici which is mainly on Capsicum but has a much wider host range.
Crop loss
In India, pepper is traditionally grown in the Western Ghats, in the states of Kerala,
Karnataka and Tamilnadu, recently it is introduced to non-traditional areas of Andhra
pradesh and North Eastern States. Foot rot has been reported from the introduced
areas such as Tripura (Sarkar et al. 1985). The crop losses due to foot rot of pepper is
reported to range up to 30 per cent (Samraj and Jose 1966, Nambiar and Sarma 1977).
Crop loss surveys conducted during 1982–1986 in two major pepper growing
districts of Kerala (Calicut and Cannanore) has shown that 3.4 per cent and 9.4 per
cent of the plants respectively are lost annually amounting to a corresponding
244 M.ANANDARAJ
production loss of 118 and 904 tons (Balakrishnan et al. 1986, Anandaraj et al.
1989a, 1989b). Every year farmers replant to compensate for the loss of plants, not
only due to disease but also due to drought. The annual crop-loss due to foot rot in
Cannanore district of Kerala remains the same as indicated by the recent survey
report, with an estimated loss of 9.2 per cent (Prabhakaran 1995). Foot rot takes a
heavy toll in all pepper growing countries and 5–10 per cent loss has been reported
in Malaysia and up to 95 per cent loss in individual gardens (Kueh and Sim 1992a),
similar situation prevails in India also.
Spatial pattern of foot rot spread

Nambiar and Sarma (1982) studied the pattern of spread of foot rot disease within a
garden over a period of six years and found that the disease spread is in centrifugal
pattern from the source of inoculum. The initial occurrence and subsequent spread of
foot rot was monitored over a two year period in a pepper plantation at Indian
Institute of Spices Research farm, Peruvannamuzhi and the data were analysed using
Spatiotemporal distance class analysis developed by Nelson (1995a, 1995b). The
analysis indicated that both initial occurrence and subsequent spread followed a
strictly non-random pattern and the infection clustered around the previously
infected plants (Anandaraj 1997) suggesting the role of initial infection serving as
the source and focus of subsequent spread (Zadocks and Van den Bosch 1994). The
root infection culminating in foot rot has a long incubation time and takes nearly 2–
3 rainy seasons. During this time the infected plants remaining in the gardens with
decline symptoms serve as a source of inoculum for subsequent spread. The foliar
infection spreads within the bush through rain splashes from the lower portions to
upper portions, whereas, spread to the adjacent plants is through both rain splashes
and also through wind blown water droplets (CPCRI 1986, Ramachandran et al.
1988c).
Influence of weather on disease incidence

Aerial infection results in defoliation and in severe cases death of plants. The spread
is dependent on the prevalence of favourable weather. The occurrence and spread of
foliar infection was studied in an arecanut-pepper mixed cropping system and
correlated with the weather factors. A combination of factors such as daily rainfall of
15.8–23.0 mm, temperature range of 22.7–29.6°C, relative humidity of 81–99 per
cent and sunshine 2.8–3.5 h /day favour the spread of aerial infection
(Ramachandran et al. 1988c, 1990). In the soil phase, the pathogen activity is
confined to the wet monsoon period and depend upon the availability of soil
moisture (Anandaraj 1997). The onset of monsoon season also triggers the growth of
pepper plants through production of new foliage and roots, maximum being in July
when the South West monsoon is at its peak. The weather conditions during monsoon
along with high soil moisture (>25%), temperature ranging from 22–29°C, relative
humidity >80 per cent, are favourable for rapid multiplication of the fungus
DISEASES 245
(Anandaraj 1997). Attempts were also made to correlate the occurrence of

Phytophthora foot rot with the weather conditions (Nair et al. 1988, Mammotty et al.
1991). Since root rot culminating in foot rot has a very long incubation period,
correlation of weather factors recorded at the time of observing foliar symptoms may
not be a correct indication of the weather requirements for disease development.
Role of weather on the growth of pepper plants

Pepper plants being perennial, the growth also depends upon the availability of soil
moisture. The production of new foliage was monitored in two cultivars of pepper,
Karimunda and Panniyur 1, by tagging the fruiting lateral branches and counting the
new leaves. Highest leaf production occurred in July in both the cultivars (Fig. 5.1.2).
Figure 5.1.2. Proportion of new leaves to old leaves observed and expected for two-year
period.
a) Karimunda first year b) Panniyur-1 first year
c) Karimunda second year d) Panniyur-1 second year
246 M.ANANDARAJ
Figure 5.1.3 Feeder root production in pepper.

a) At three distances b) At three depths
Feeder root production was estimated by soil core method by collecting soil cores at
20, 40 and 60 cm away from the base of the vine and at 20, 40 and 60 cm depth at each
distance at monthly intervals. Highest feeder root production was in July and the
DISEASES 247
feeder roots were concentrated at 0–40 cm from the base of the vine upto 40 cm depth
(Fig. 5.1.3). A similar pattern of feeder root concentration was reported from
Indonesia. Ipor et al. (1993), while studying root architecture of pepper in Indonesia,
recorded 63.8 per cent of feeder roots in the top 0–50 cm. Thus, production of the
most susceptible tender tissues, both foliage and feeder roots, occur at the peak
monsoon season (Anandaraj 1997). The wet monsoon season in India, not only
activate the pathogen but also affects the growth of the host plant. Growth of host
indirectly influence the pathogen by the increased root exudation and availability of
more susceptible tissues for colonization.
Survival
In the soil phase contaminated soil is the main source of inoculum. The inoculum
survives in the soil up to 19 months in the absence of host plant (Kueh and Khew 1982,
CPCRI 1986). The soil inoculum was monitored by Ramachandran et al. (1986) in a
pepper plantation by collecting soil samples at various depths and distance from the
infected vine. The study has shown that the pathogen was concentrated on the surface
0–30 cm and it gets reduced as the distance and depth increase from the source of
diseased plant. The main survival structures of P. capsici in the soil are chlamydospores
and thickened mycelium (Anandaraj 1997). Soil moisture was found to have a positive
correlation on the activity of the fungus in soil. P. capsici has a low competitive
saprophytic ability, hence addition of organic amendments to soil promotes growth of
saprophytic organisms which in turn reduce the populations of P. capsici (Anandaraj
1997). Production of oospores under laboratory conditions and their possible role in
the disease have been suggested (Sastry 1982, Sastry and Hegde 1987a, 1987b, 1988,
Santhakumari 1987). Trichoderma viride stimulate oospore formation and also when
two compatible types are inoculated on to pepper (Brasier 1969, 1978, 1991). However,
oospores as resting structures in infected plant tissues has not been recorded from India.
Oospores as survival structures have been recorded in Sarawak and were found to be
viable after passing through the alimentary canal of snail (Kueh and Khew 1982). A
technique for germinating the oospores of Phytophthora by passing the oospores
through the guts of snail has been suggested (Dutta et al. 1984).
Disease resistance
Screening the germplasm of pepper is done adopting stem and root inoculation
techniques (Nambiar and Sarma 1979, Sarma et al. 1994). Root inoculation is done by
dipping the root system in zoospore suspension while the stem inoculation consists of
inoculating the fungus at the third internode of a pepper cutting with 4–5 leaves. The
fungus, in the form of 5 mm diameter mycelial disc cut from the edge of a 48 h old culture,
is placed at the third internode with a pin prick and covered with moist cotton wad and
incubated in humid chamber. Observations are recorded after 72 h on the lesion size and
depth of penetration. The lesion size range from 5 mm–120 mm, and depth of penetration
can confine to surface or can lead to the rotting of the entire internode. After 72 h of
248 M.ANANDARAJ
incubation under humid conditions, those cuttings showing lesion size of less than 5 mm
and penetration restricted to the surface are rated as tolerant and preserved for future work.
In India, all the cultivated germplasm are susceptible to this disease. Among the cultivars,
Narayakkodi, Kalluvally, Balankotta, Neelamundi, Mundi and Uthirankotta have been
identified as tolerant (Sarma and Anandaraj 1997). Among other taxa, Piper colubrinum,
a distant South American species, is highly resistant to P. capsici. Several open pollinated
progenies of Perambramundi, Kalluvally Cholamundi and hybrids involving Panniyur
1×Karimunda, and Narayakkodi×Neelamundi have recorded tolerant reaction (Sarma et
al. 1994). In Malaysia, Cheriakaniakadan and Balankotta were less susceptible than
Kuching. Whereas in Indonesia cvs. Kalluvally, Palau Lauta, Belantung, Bangka, Natar
I, Merefin, Banjarmasin and Duanteber were rated as less susceptible (Sitepu and Kasim
1991, Manohara et al. 1992). In India, currently, researches are directed to understand the
mechanism of tolerance to P. capsici. Among the biochemical parameters, the ratio of total
phenols to orthodihydroxy phenol (OD phenols) was higher in susceptible cultivars than
in tolerant cultivars. Higher peroxidase activity was recorded in P. hirsutum, a
Phytophthora resistant line, and low levels in Daun Leber, a susceptible cultivar
(Rahayuningsih 1990). Regeneration protocol for pepper has already been developed so
as to attempt biotechnological methods for transferring resistance to the cultivated
varieties (Shaji et al. 1995a, 1995b, 1996, Sarma et al. 1996).
Disease Management
An integrated disease management involving cultural, chemical and biological
control is recommended (Ramachandran et al. 1991, Sarma et al. 1988, 1992b,
Anandaraj and Sarma 1995, Sarma and Anandaraj 1997).
Cultural control
Provision of drainage: Population build-up of P. capsici is dependent on weather and
is positively correlated with soil moisture (Anandaraj 1997). High precipitation
during rainy season leads to water logged conditions. Such conditions predispose
plants to Phytophthora infections. During water stagnation, temporary anaerobic
conditions result in low oxygen and together with increased root exudation
stimulates germination and growth of pathogen propagules. Such conditions
enhance host susceptibility due to decreased production of phenol oxidases, reduced
phytoalexin production, suppression of mycorrhiza and reduction in nitrogen
fixation (Drew and Lynch 1980). Thus adequate drainage is essential to reduce the
population build-up of P. capsici and subsequent infection of pepper plants.
Phytosanitation
Pepper Phytophthora is reported to survive up to 19 months in plant debris. The
initial occurrence and spread of the disease is also non-random and tend to cluster
around the previously infected plants (Anandaraj 1997), hence the infected plants
serve as the foci of infection (Zadocks and van den Bosch 1994). Removal of infected
plants would reduce the inoculum level and spread of the fungus.
DISEASES 249
Shade regulation
Pepper is trailed on live supports like Erythrina indica, Garuga pinnata, Glyricidia
sepium etc. During monsoon season the canopies of the support trees also grow and
generate a microclimate under their canopies with high humidity and low
temperature, which is ideal for P. capsici to multiply and infect. Lopping of the
branches during rainy season is essential to facilitate penetration of sunlight and
reduction of high humidity thereby altering the microclimate. The lopped branches
could be used as mulch to prevent soil splashes.
Cover crops
The main source of initial inoculum of P. capsici in pepper plantation is the
contaminated soil. Infection on the foliage occurs through soil splashes often
initially to the tender shoots trailing on the ground, and from these shoots to other
parts of the canopy through rain splashes (Ramachandran et al. 1990). To prevent soil
splashes live mulch in the form of legume and grass cover are suggested
(Ramachandran et al. 1991, Sarma et al. 1992c). But, recent studies have shown that
population of P. capsici increases under weed cover and death of plants is faster with
weeds than without weeds (Anandaraj 1997). Although weed cover reduces soil
splashes and restrict movement of propagules along with soil, it also supports the
population build-up of P. capsici. In Malaysia, studies with Desmodium trifolium as
cover crop for pepper has indicated that plants showed faster and better growth in
clean weeded plot than with cover crop and concluded that it was economical to
grow pepper in clean weeded plot (Ahmed 1993). In India, after the monsoon, there is
a prolonged drought from November to May. During this period weeds compete for
soil moisture and the population of P. capsici also survives longer. Hence, after the
rainy season it is better to remove the weeds in pepper plantations and rake up the top
soil. Removing weeds and turning the top soil would help to conserve soil moisture,
as the capillary pores are broken (Brady 1984, Russell 1973) and soil moisture
removal by weeds during summer is also reduced. Once weeds are removed the
saprophytic survival of P. capsici on weeds would also be reduced. In view of this, a
post monsoon clean cultivation is suggested (Anandaraj 1997). Root exudates of
some of the plants such as Allium spp. are inhibitory to zoospores of Phytophthora
(Manohara et al. 1992). Aqueous extracts of P. colubrinum, Azadirachta indica,
Strychnos nuxvomica, Lantana camera extract and Chromolaena odorata
(Eupatorium) were tried on P. capsici and C. odorata extract was found toxic to P.
capsici (Anandaraj and Leela 1996). Mulching with this plant has been reported to
increase the yield in Cambodia (Litzenberge and Lip 1961). Although the mulching
was done to reduce the nematode infestation on pepper, there was no reduction in the
nematode population but recovery of plants have been reported.
Chemical control
Although the disease occurs every year during rainy season, a fixed fungicide
scheduling is advocated against both aerial infection and collar infection. The control
250 M.ANANDARAJ
measures include: spraying of Bordeaux mixture 1 per cent (BM), pasting the collar
with BM and drenching the basins with either BM or with copper oxychloride
(Ramachandran et al. 1991, Sasikumaran et al. 1981, Nair and Sasikumaran 1991,
Malebennur et al. 1991, Lokesh and Gangadarappa 1995). Based on the
epidemiological studies and nature of occurrence of collar infection, the practice of
pasting the collar with Bordeaux mixture is discouraged (Anandaraj et al. 1994, 1996a,
1996b, Sarma et al. 1992c). Among the systemic fungicides, several formulations of
metalaxyl such as Ridomil granules and Ridomil-ziram have been reported to be
effective against foot rot of pepper (Ramachandran and Sarma 1985, Ramachandran
1990, Ramachandran et al. 1988b, 1991, Sarma et al. 1992c, Kueh and Sim 1992a,
Kueh et al. 1993). In experiments with granular formulations of Metalaxyl, Ridomil 5G
at 50 g per plant gave protection up to seven weeks and granular formulations were
better than foliar spray (Kueh et al. 1992, 1993). However, owing to the cost of systemic
fungicides and the poor socioeconomic conditions farmers seldom use them. While
reviewing the control of four soil-borne Phytophthora diseases, doubts about the
success of chemical control of Phytophthora foot rot was expressed by Coffey (1991).
Studies with various concentrations and frequency of application revealed that it is
safe to apply the chemical six months prior to harvest to prevent the traces of metalaxyl
residues in the final product (Sarma et al. 1992c).
Use of beneficial microorganisms

Several beneficial organisms like vesicular arbuscular mycorrhizae (VAM) are
associated with pepper (Ramesh 1982, Manjunath and Bagyaraj 1982).
Incorporation of VAM alone or in combination with other beneficial microorganisms
like Azotobacter and Azospirillum enhance rooting and growth of pepper (Govindan
and Chandy 1985, Bopaiah and Khader 1989). VAM inoculation has been found to
enhance rooting, growth and suppress root damage caused by P. capsici, R. similis
and M. incognita under artificial inoculation and under field conditions (Anandaraj
and Sarma 1994a, Anandaraj et al. 1991a, 1991b, 1996c, Sivaprasad et al. 1990a,
1990b, 1995). Occurrence VAM has been a rule rather than an exception in crop
plants (Harley 1989). Colonization of mycorrhiza alters the nature of root exudate
and the rhizosphere microflora due to the influence of mycorrhizosphere effect
(Dehne 1982, Linderman 1988, Graham 1982,1988).VAM fungi have been reported
to suppress the root rot caused by Phytophthora in citrus (Davis and Menge 1981,
Davis et al. 1978, 1980). VAM fungi not only enhance growth but also suppresses
diseases caused by soilborne pathogens (Ewald 1991, Graham and Egel 1988).
Colonization by VAM is described as a prelude to biological control. Realizing the
importance of this, incorporation of VAM in the nursery is recommended both for
enhancing growth and suppressing root infection (Sarma et al. 1996).
Organic amendments
Organic matter such as neem oil cake (Sadanandan et al. 1992, Nair et al. 1993)
soyabean meal, ground nut cake, coconut cake and chicken manure are added to the
DISEASES 251
soil to supplement nutrition and enhance the growth of saprophytes (Kueh and Sim
1992a). In soils amended with organic matter the saprophytic activity is enhanced
and P. capsici population drops to undetectable levels (Anandaraj 1997).
Biological control
Soil borne pathogens are amenable to biological control (Cook and Baker 1983). In
the rhizosphere of pepper several antagonistic microorganisms belonging to
Trichoderma and Gliocladium occur (Dutta 1984, Anandaraj and Sarma 1994b,
Anandaraj and Peter 1996). P. capsici being soilborne, and the main source of
inoculum is contaminated soil, growth of antagonistic fungi would prevent the
population build up. The competitive saprophytic ability of P. capsici is very low
and addition of organic matter to the soil containing P. capsici promotes the growth
of saprophytes and reduces the population of P. capsici (Anandaraj 1997). Several
strains of biological control agents effective in protecting pepper against P. capsici
have been isolated, screened and mass multiplied on inexpensive carrier media and
applied in the field with promising results (Anandaraj and Sarma 1995, Sarma et al.
1996). Mature coconut water, which is an agricultural waste, supports good growth of
Trichoderma and Gliocladium and could be used for the mass multiplication of these
antagonistic fungi (Anandaraj and Sarma 1997).
Thus integrated control involving phytosanitation, cultural, chemical and biological
controls are being followed to check Phytophthora infections in pepper (Ramachandran
et al. 1988a). Attempts are also being made to incorporate resistance in the cultivars by
adopting biotechnological means. For this the necessary regeneration protocols have
already been developed (Shaji et al. 1995a, 1995b, 1996).
Fusarium Wilt of Pepper

In Brazil, the major disease that is creating havoc to pepper cultivation is the
Fusarium wilt, and this disease is causing severe losses in that country (Duarte and
Albuquerque 1991).
Root rot and stem blight

The symptoms of Fusarium infection is root rot leading to flaccidity and yellowing
of foliage. The affected plants are killed within a short period. The organism is
identified as Fusarium solani f. sp. piperis. The perfect stage has been identified as
Nectria haematococca f. sp. piperis. In affected plants the fungus produces abundant
perithecia. Fusarium infection in plantation is reported to reduce the economic life
of plantation from 20 to 6–8 years and the productivity per plant from 3.0–1.5 kg
(Duarte and Albuquerque 1991).
Disease management
Phytosanitary measures like removing infected plants and burning and application
of 200 g calcium cyanamide per mound are practiced. Chemical control measures
252 M.ANANDARAJ
with both systemic and contact fungicides are resorted to depending on the nature
of damage. Benomyl, carbendazim and thiobendazole at 0.5 and 0.6 per cent are
reported to be effective against Fusarium. Prophylactic application of fungicides
at fortnightly interval, systemic fungicide followed by contact fungicide to the
foliage and soil drenching with Benomyl (0.05%) and thiobendazole (0.06%) were
found effective in controlling the disease. In the nursery, benomyl or
thiobendazole at 500 ppm for Fusarium and metalaxyl at 500 ppm or Bordeaux
mixture at 10,000 ppm for Phytophthora infections, Pencycuron 500 ppm for
Thanatephorus cucumeris are followed. None of the cultivars was found resistant
whereas, Piper attenuatum, P. cariconnectivum, P. betle and P. colubrinum were
resistant (Duarte and Albuquerque 1991). Mutation breeding by irradiation of
seeds was found promising (Poltronieri et al. 1991). [Note: The etiology of this
disease is still not completely understood. Holliday informed that he has not come
across any proper evidence that any Fusarium sp. causes a wilt of any virulence
anywhere. More studies are needed to establish the Fusarium etiology beyond
doubt (Holliday, private communication, ed.]
Slow Decline of Pepper

Slow decline disease of pepper is a debilitating disease, where the affected plants
survive for several years and death of plants occur gradually over a period of 3–4
years. This disease was earlier referred to as “slow wilt” (Nambiar, 1978, Nambiar and
Sarma 1977, Sarma and Nambiar 1982) as slow decline in Malaysia (Kueh and Sim
1992c, Varughese and Anuar 1992) and “Yellow disease” (De Waard 1979, Zaragoza
et al. 1991) or “Yellows disease” in Indonesia (Sitepu and Kasim 1991). Studies on
the etiology has shown that this disease is caused by feeder root damage by
Phytophthora capsici, Radopholus similis and Meloidogyne incognita either alone
or in different combinations (Anandaraj et al. 1996a, 1996b). (For details see the
chapter on nematode induced diseases)
Anthracnose of Pepper
Anthracnose in pepper is referred to as “pollu” disease in India, which means hollow
fruits and as black berry disease in Malaysia and Indonesia. This occurs both on the
leaves and on spikes. Although sporadic in nature in the major pepper growing state
of Kerala, this disease is becoming severe in parts of Karnataka where pepper is grown
on shade trees in coffee plantations.
Symptoms
The symptoms on fruits depend on the stage of maturity. On younger fruits infection
lead to blackening. On mature fruits brownish lesions are formed (Ayyar et al. 1918,
Sebastian 1982). If the infection occurs on the stalk end of spike, the entire spike is
shed prematurely, and brown lesions are produced on the leaves.
DISEASES 253
Etiology
The fungus Colletotrichum necator is the cause of this disease (Rao 1926, Thomas
and Menon 1939). From India, Colletotrichum sp., C. gloeosporioides are also
recorded. The severity of the disease vary and a range of 28–34 per cent has been
reported causing a crop loss of 1.9–9.5 per cent (Nair et al. 1987). The fungus is
reported to survive on Dioscorea triphylla as an alternate host (Wilson 1960).
Disease Resistance
There is no report of resistance to this disease. In a mixed cropping system
experiment involving coconut and five cultivars of pepper, all five cultivars have
been reported to show disease incidence. Berry infections recorded were 9.3, 9.8,
16.3, 19 and 23.2 per cent in Karimunda, Kottanadan, Narayakkodi, Balankotta and
Panniyur-1 respectively (Radhakrishnan and Nair 1983). Panniyur-1 recorded
highest incidence followed by Balankotta.
Disease management
As the disease occurs during the rainy season, Bordeaux mixture (1%) spray is
recommended (Sundararaman 1928, Nair et al. 1987). Apart from Bordeaux mixture
spray, Difolatan at 0.2 per cent was also reported to give adequate control. In Sarawak,
Benomyl, Thiophanate ethyl, Thiophanate methyl, Carbendazim, Captofol and
Tridemefron were also effective in controlling this disease. Anthracnose is reported to
be reduced when 40 per cent shade is provided by using shade nets (Kueh et al. 1993).
Stunted Disease
This disease, also known as little leaf disease, was recorded during 1975 in Idukki
district of Kerala which is one of the major pepper producing areas (Pailey et al.
1981). Earlier it was sporadic, but now found in all major pepper growing tracts of
Kerala and Karnataka. A survey has indicated that number of plants affected in
Wynad district of Kerala ranged from 0.6 to 18.6 per cent (NRCS, 1994). This disease
is known as mosaic disease (Prakasam et al. 1990) and as “little leaf” in Sri Lanka
(Randombage and Bandara 1984), mosaic disease in India, (Prakasam et al. 1990)
“wrinkled leaf disease” in Malaysia (Kueh and Sim 1992b) and as “stunted disease”
in Indonesia (Sitepu and Kasim 1991, Firdausil et al. 1992).
Symptoms
In severely affected plants the symptoms are as follows. The leaves become narrow
and leathery in texture, with puckering and chlorotic streaks, internodes become
shortened and the branches appear as witches broom, at times the leaves show
narrowing and vein banding. The appearance of symptoms are pronounced in
neglected gardens and older plants recovering after slow decline infection. In the
254 M.ANANDARAJ
nurseries, chlorotic streak and vein banding are more common. Kueh and Sim (1991)
differentiated four categories of symptoms namely, stunting, reduction in size of
internodes, narrowing of leaves, marginal necrosis and chlorosis. Detailed studies on
morphology of healthy and infected plants has shown reduced height, girth of
column, internode length and leaf area (Eng et al. 1993).
Etiology
Transmission tests carried out in India has shown that the disease is graft
transmissible. ELISA tests indicated that the disease is caused by cucumber mosaic
virus (CMV). Recent electron microscopic studies showed CMV particles in the
infected tissues and it is concluded that the disease is caused by cucumber mosaic
virus (IISR 1995, 1997, Sarma et al. 1992a). In Malaysia, based on serology tests and
fluorescent microscopy the involvement of cucumber mosaic virus and chilli veinal
mottle virus were ruled out (Eng et al. 1993). Studies with immunosorbant electron
microscopy, transmission electron microscopy using ultra thin sections also did not
reveal the presence of virus in infected tissues. However, purified extracts have been
reported to contain bacilliform virus particles measuring 120×30 nm, isometric virus
of 30 nm and rod shaped virus related proteins. Gel electrophoresis also reported to
show the presence of ds RNA indicating plant viruses. Based on this study presence
of badna virus transmitted by mealy bugs and clostero virus are reported (Eng et al.
1993). Recently Lockhart et al. (1997) have shown that a previously undescribed
Badna virus is a causal agent of this disease. The virus named as Piper Yellow Mottled
Virus (PYMV) has non-enveloped bacilli-form virions, averaging 30×125 nm in size
and containing double stranded DNA genome. The virus is transmissible
mechanically as well as by citrus mealy bug.
Disease management
Presently, roguing of infected plants and following quarantine measures to prevent
introduction of this disease to disease free areas are recommended
MINOR DISEASES
Phyllody
This disease has been reported from Wynad district of Kerala which is a major pepper
growing area (Sarma et al. 1988, Sarma and Anandaraj 1992), this is also called as
antholysis (Remila and Neelakandan 1994).
Symptoms
The spikes and flowers are converted into leaf-like structures instead of normal
flowers and the stalk of the affected spikes are also elongated. The leaves of the
DISEASES 255
affected plants become smaller and shows chlorosis. In the same vine both normal
spikes and berries are also produced.
Etiology
Based on electron microscopic studies, the disease is reported to be caused by
phytoplasma (Sarma et al. 1988, 1991).
Disease management
As the disease is confirmed to be caused by phytoplasma, removal of affected plants
and following of quarantine measures are suggested (Sarma and Anandaraj 1992).
Bacterial Leaf Spot

This disease is caused by Xanthomonas compestris pv betlicola and occurs
sporadically in certain pockets (Mathew et al. 1978) and in the vicinity of other
Piper spp. (Bhale et al. 1984). The causal organism is Xanthomonas compestris. The
symptoms appear as small water soaked lesions on the leaf lamina and margins which
later become dark with a chlorotic halo and at time cause defoliation.
Chloramphenicol at 200 ppm was reported to be effective in inhibiting the growth of
the bacterium (Mathew et al. 1979). However, control measures to prevent this
disease in the field are not available.
Thread Blight
This disease occurs on pepper leaves and spikes (Ramakrishnan 1957). The fungus
grows underneath the leaves and on stem causing drying up of leaves and spikes.
Pellicularia filamentosa (Corticium solani) is reported as the causal organism.
Stump Rot
The occurrence of stump rot caused by Rosellina bunodes was recorded by Menon
(1949) in Wynad areas of Kerala. The fungus affects the root system which results in
drying up of plants. The fungus also affect Grevillea robusta on which pepper plants
are trailed. Isolation of affected plants by making trenches is recommended to
prevent the spread of the disease to adjacent plants.
Red Rust
Red rust caused by the alga Cephaleuras mycoidea occur on older leaves in certain
pockets. This was reported to cause black fruit in Malaysia (Menon 1949, Sarma et al.
1991). This occurs on the surface of leaves, there by cutting off light required for
photosynthesis. The exact nature of damage has not been assessed. When the growth
occcur on the spikes and fruits the appearance of the berries are affected and the
quality is reduced.
256 M.ANANDARAJ
Dodder
The occurrence of parasitic flowering plant (Cuscuta reflexa-Convolvulaceae) on
pepper is recorded in some pepper growing areas. Affected plants are fully covered by
the parasite and the productivity of the vine is affected. Removal of the affected
branches is the suggested control measure (Sarma et al. 1991).
Velvet Blight
The velvet blight is caused by Septobasidium sp. The fungus grows on the surface of
the fruits and forms a coating but does not penetrate the fruits. Whereas, when it
occurs on the branches it results in die back symptoms. Pruning of the affected
branches would prevent the spread of the fungus (Sarma et al. 1991).
White/Yellow spots
White/Yellow spots occurs on the stem and are caused by lichens. Brown spots
caused by unknown pathogen have been recorded on pepper (Sarma et al. 1991).
These diseases seldom occur and do not cause serious losses. No detailed information
is available on them.
NURSERY DISEASES
Black pepper is propagated vegetatively through cuttings. Three types of planting
materials are used for propagation. In the first type orthotropic terminal shoots are
taken from the plants during rainy season and planted directly in the field. In the
second type, the runner shoots which are produced from the base of the vine during
rainy season, are allowed to trail on the ground or are kept coiled around the base of
plants and taken at the time of producing the cuttings. The third type, the cuttings are
allowed to trail on 1.2 m long bamboo splits filled with potting mixture and arranged
in an angle of 45°. As the vine grows, it is tied to the bamboo split to ensure contact
with the potting mixture. Roots are produced at each node and when the cutting has
grown to the length of the bamboo split, the plants are cut from the bottom leaving 2–
3 nodes and cut into bits, each node with a leaf and roots,and planted in individual
polythene bags (Sivaraman 1991). In the latter method cuttings are produced the year
round and the conditions are favourable for the diseases to develop. Depending on
the type of nursery the disease problems also vary.
Leaf Rots and Blights

In the nurseries raised using the runner shoots, stem cuttings with 2–3 nodes are
planted in polythene bags containing nursery mixture made up of forest soil, sand
and farm yard manure in the proportion of 1:1:1. As the cuttings sprout, several
diseases such as leaf spots and blights develop on the young sprouts. Rhizoctonia sp.
DISEASES 257
cause greyish sunken spots on the leaves and infected leaves remain attached to one
another. The spots caused by Colletotrichum sp. are characterized by yellowish halo
surrounding the necrotic spots. (Mammootty et al. 1980, 1992; Mammootty and
Pillay 1981).
Basal Wilt
Invasion of Sclerotium rolfsi on pepper seedlings in the nursery causes rotting and
wilting of the cuttings. The affected plants show greyish lesions on stems and growth of
the fungus as whitish mycelium with numerous sclerotia. On the leaves greyish spots
with whitish mycelium at the advancing edges of lesion and sclerotia on lesions are
seen. Carbendazim and mercuric fungicides are reported to be effective in checking the
germination of sclerotia under in vitro tests (Choudhury 1943, Brahma et al. 1980).
Phytophthora Infections
Phytophthora infections are severe during rainy season when the cuttings are
exposed to rain. Infection occurs on leaves, stem and roots. Infection starts as spots on
the tender leaves with the characteristic fimbriate advancing margin and the leaves
are blighted within 2–3 days and spread to the adjacent cuttings through rain
splashes. Infection on the stem results in withering of the entire cutting. Root
infection results in sudden wilting of the cutting. The inoculum for the outbreak of
Phytophthora infections is carried from diseased gardens inadvertently to the
nursery in the form of incipient infection on the roots of runner shoots and passively
in the form of soil particles adhering to the runner shoots. In case of rapid
multiplication in nurseries, as the conditions are favourable year round infection can
occur.
Disease Management in Nurseries

Pepper being a perennial crop, producing disease free planting material is the first
step in disease management. P. capsici, which occurs on all parts of pepper and infect
all stages of the plants, calls for greater precaution to prevent the introduction of the
fungus to newer areas. The disease management strategy includes collection of
disease free planting material, disinfection of nursery mixture and an integrated
control measures (Sarma et al. 1988a, 1988b, Anandaraj and Sarma 1995).
Collection of planting material

Runner shoots used for multiplication must be collected from disease free gardens.
The roots present on the runner shoots which were trailing on the ground has to be
removed and the material washed throughly with water to remove all the adhering
soil particles and the cuttings dipped in a fungicide such as Mancozeb or any copper
fungicide before planting in polyethylene bags.
258 M.ANANDARAJ
Preparation of nursery mixture

After preparing the mixture it may be sterilized using methyl bromide or through
solarization by spreading the mixture in an open area up to a height of 30 cm,
moistening with water and covering with polyethylene sheet (Sarma et al. 1996).
After solarization, the mixture is fortified with vesicular arbuscular mycorrhizae and
antagonistic fungi like Trichoderma and Gliocladium. As the cuttings grow and show
symptoms of infection, infected cuttings are separated and a prophylactic spray with
a fungicide such as Bordeaux mixture (1%) is given to prevent the spread of the
disease (Mammootty et al. 1980, Mammootty and Pillay 1981, Mammootty et al.
1992, Sarma et al. 1988a, 1988b). To protect the cuttings from Phytophthora a foliar
spray with 200 ppm of metalaxyl was found very effective. Metalaxyl is compatible
with biocontrol organisms, and application of biocontrol agents to the soil together
with spraying the foliage with metalaxyl would offer better protection. In short,
nursery diseases could be managed by using cuttings from healthy gardens, by
adopting phytosanitation and spraying the cuttings with Bordeaux mixture (1%) or
metalaxyl 200 ppm as and when such necessity arise.
CONCLUSIONS
In pepper all the fungal diseases described above occur during the wet monsoon
season under Indian condition. In other pepper growing areas also Phytophthora
infections occur during the wet period. Although the weather requirement for
Phytophthora diseases are studied in detail, in the integrated management of
diseases a fixed fungicide schedule is followed as the favourable weather conditions
are attained during the monsoon period every year. The fungicide application to the
foliage at the onset of monsoon would protect the plants against the infections
caused by Phytophthora, Colletotriehum etc. The application of organic manures
along with biocontrol agents would prevent the population build-up of P. capsici in
soil and protect the roots against the damages. Present research efforts are
concentrated on host resistance, by understanding the mechanism of resistance and
incorporating the same through biotechnological means, so that host resistance
becomes an important component of integrated management of diseases of pepper.
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5.1.

DISEASES OF BLACK PEPPER

Indian Institute of Spices Research, Kozhikode-673 012, Kerala,

Phytopbthora Diseases in Pepper

Symptoms of foliar infection

Symptoms on roots and collar

Etiology of Phytophthora foot rot

Figure 5.1.1 Symptoms due to Phytophthora capsici infection on black pepper

identified as Phytophthora palmivora var piperis (Samraj and Jose 1966), P.

Identity of the pathogen

Isolation from soil

Biology of the pathogen

Taxonomy of pepper Phytophthora

Spatial pattern of foot rot spread

Influence of weather on disease incidence

(Anandaraj 1997). Attempts were also made to correlate the occurrence of

Role of weather on the growth of pepper plants

Figure 5.1.3 Feeder root production in pepper.

Use of beneficial microorganisms

Fusarium Wilt of Pepper

Root rot and stem blight

Slow Decline of Pepper

Bacterial Leaf Spot

Leaf Rots and Blights

Disease Management in Nurseries

Collection of planting material

Preparation of nursery mixture

of Phytophthora palmivora (Butl.) on hosts of high intensity cropping systems in upcountry

Manohara, D. and Sato, N. (1992) Morphological and physiological observations on the

In M.Anandaraj, and K.V.Peter, (eds.), Biological Control in Spices, Indian Institute of

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