Botanical Studies (2009) 50: 1-10.

*

Corresponding author: E-mail: kowh@dragon.nchu.edu.tw;

Tel: 886-4-2284-0780; Fax: 886-4-2287-7585.

CONTENTS

INTRODUCTION ................................................................................................................................................................... 1

HISTORY OF MACADAMIA DECLINE .............................................................................................................................. 2

Slow decline ........................................................................................................................................................................ 2

Quick decline

....................................................................................................................................................................... 3

DETERMINATION OF THE CAUSES OF DECLINE PROBLEMS ................................................................................... 3

Slow decline ........................................................................................................................................................................ 3

Quick decline

....................................................................................................................................................................... 4

SYMPTOMS AND SIGNS OF SLOW AND QUICK DECLINE .......................................................................................... 6

Slow decline ........................................................................................................................................................................ 6

Quick decline

....................................................................................................................................................................... 6

INOCULUM SOURCES AND INITIAL INFECTION .......................................................................................................... 7

Slow decline ........................................................................................................................................................................ 7

Quick decline

....................................................................................................................................................................... 7

MODES OF DISEASE DEVELOPMENT RESULTING IN SLOW AND QUICK DECLINE ............................................ 8

Slow decline ........................................................................................................................................................................ 8

Quick decline

....................................................................................................................................................................... 8

Decline caused by multiple infections

................................................................................................................................. 8

DISEASE MANAGEMENT ................................................................................................................................................... 8

CURRENT STATUS AND FUTURE OUTLOOK ................................................................................................................. 8

LITERATURE CITED

............................................................................................................................................................. 9

INTRODUCTION

Macadamia (Macadamia integrifolia Maiden & Betche)

is a beautiful, evergreen tree that usually attains a height of

Nature of slow and quick decline of macadamia trees

Wen-Hsiung KO*

Department of Plant Pathology, National Chung Hsing University, Taichung, Taiwan

(Received May 5, 2008; Accepted July 4, 2008)

ABSTRACT.

Macadamia which is native to Australia has been grown in commercial scale in many counties

after its development into an economic crop in Hawaii in the 1930s. Tree decline is the most serious problem

in macadamia plantations. It consists of slow decline resulting from root rot caused by Kretzschmaria clavus

or Ganoderma lucidum and quick decline resulting from trunk decay caused by Nectria rugulosa, Xylaria

arbuscula, Phellinus gilvus, Phytophthora tropicalis, or Acremonium recifei. Inoculum sources and modes of

disease development differ due to difference in causal organisms. A diagnostic key for slow and quick decline

of macadamia trees is presented.

Keywords: Acremonium recifei; Ganoderma lucidum; Kretzschmaria clavus; Macadamia integrifolia; Nectria

rugulosa; Phellinus gilvus; Phytophthora tropicalis; Xylaria arbuscula; Quick decline; Slow decline.

REVIEW PAPER

20 m and a crown diameter of 13 m (Figure 1A). Its nuts

are renowned as being among world¡¦s most delicious. In

addition to the popularity of chocolate-covered macadamia

nuts, whole kernels of macadamia are sold as oil-roasted

or dry-roasted snack nuts while broken kernels are used

as an ingredient in ice cream, cookies, bread, cake, pie,

muffins, wafers, and fresh vegetable salads.

2

Botanical Studies, Vol. 50, 2009

Macadamia is native to subtropical eastern Australia

where many homeowners have planted it around their

homes for shade, as a source of nuts, and to enhance

the beauty of their properties. The University of Hawaii

developed its potential as an economic crop in the 1930s.

The number of macadamia farms increased steadily, and

macadamia nut has gradually become one of the highest

commodities by value in Hawaii. In 1989, a record

22,500 tons of nuts were harvested from approximately

22,300 acres in Hawaii for a record farm value of $44.9

million (Crop Knowledge Master, 2005). The Hawaiian

success encouraged other countries to grow macadamia

on a commercial scale in the 1950s, and since 1970, the

area under cultivation has increased rapidly, with large-

scale plantings in many countries including Australia,

South Africa, Guatemala, Kenya, Malawi, Costa Rica,

Brazil, Mexico, and China (Agroforestry Tree Database,

2006). In 1997, Australia overtook Hawaii to become the

world¡¦s largest producer of macadamia nuts. The country

harvested 34,000 tons of nuts in 1998 /1999 (USDA

Foreign Agricultural Service, 2002). Test planting of

macadamia trees in Taiwan commenced in the 1970s.

Even though conditions for growth and nut production

were very favorable, planting acreage has not increased

because of the threat of damage by typhoons. The brittle

wood and lack of clearly defined taproot make macadamia

trees particularly sensitive to damage and blow-down in

strong winds (Quinian and Wilk, 2005; Agroforestry Tree

Database, 2006).

Grafted seedlings are planted in commercial macadamia

orchards, and Hawaiian selections are the most important

cultivars planted in all macadamia-producing countries

(Allen, 1995). Grafted trees begin bearing in 5 years and

take about 10 years to reach maturity and maximum nut

yield. In Hawaii some trees over 60-years-old are still

producing. Macadamia racemes consist of small, white,

tasseled flowers growing on long spikes (Figure 1B). Fruits

are globose, consisting of a white edible kernel surrounded

by a hard seed coat covered with a thick fibrous pericarp

(Figure 1C).

HISTORY OF MACADAMIA DECLINE

Slow decline

Light brown discoloration and chlorosis of leaves on

some branches of trees followed by gradual defoliation

and development of dieback symptoms (Figure 2A) were

noticed in the 1960s in macadamia orchards near Hilo on

the island of Hawaii, the major macadamia-nut-producing

Figure 1. Macadamia trees (A), raceme (B), and immature nuts

(C).

F igure 2. Slow decline of macadamia caused by

Kretzschmaria clavus. A, a m acadamia tree showing charac-

teristic symptoms of leaf chlorosis, defoliation, and branch

dieba ck assoc iated wit h slow decli ne; B, c ross se ction of

a partially de cayed root with distinct black zone lines; C,

fruiting bodies of K. clavus produced on the surface of basal

trunk.

KO ¡X Nature of slow and quick decline of macadamia trees

3

area in Hawaii (Ko et al., 1977). The decline was relatively

slow, it taking more than 10 years for the affected trees

to die. The decline occurred only on trees over 3 years

of age. The incidence and severity of macadamia decline

were positively correlated with tree age. In an orchard

surveyed, the percentage of trees with dieback symptoms

was 9% for those 6 years of age, and more than 80% for

those 25 years of age (Ko et al., 1977). Slow decline was

considered the most serious production problem in Hawaii

before the occurrence of quick decline in 1986. In 1988, a

slow decline of macadamia trees also was reported from

Taiwan (Ann and Ko, 1988).

Quick decline

In 1986, the foliage color of the entire canopy of some

macadamia trees in a large orchard at Keaau on the island

of Hawaii changed subtly from dark green to light green.

Within 2 to 3 months, the leaf color started to turn light

brown (Figure 3A), and within a month the whole canopy

turned brown and the tree died (Figure 3B). Some trees

adjacent to the affected ones began to show the same

progression of symptoms and the number of dead trees

increased rapidly (Figure 3C). Subsequently, quick decline

of macadamia trees also occurred in orchards located in

the northeastern and western sides of the island, and on the

island of Maui. It has become the most serious production

problem of macadamia in Hawaii. In 1998, about 5,000

trees were lost to macadamia quick decline. Responding to

a desperate need by the macadamia industry, the College

of Tropical Agriculture and Human Resources of the

University of Hawaii formed a committee consisting of a

horticulturist, two entomologists, and a plant pathologist

to investigate the cause of the problem.

DETERMINATION OF THE CAUSES OF

DECLINE PROBLEMS

Slow decline

The problem of slow decline of macadamia trees

was originally considered due to a deficiency of certain

essential elements (Shigeura and Bullock, 1973).

Phytophthora cinnamomi Rand, which is widely

distributed on the island of Hawaii, has been reported to

cause macadamia trunk canker in Hawaii (Hine, 1961).

However, the disease is not of common occurrence and is

not associated with macadamia decline (Ko and Kunimoto,

Figure 3. Quick decline of m acadamia. A, a macadamia tree

showing color fading and browning of leaves before sudden

death; B, a macadamia tree that died suddenly as the result

quick decline; C, a macadamia orchard devastated by quick

decline.

Fig ure 4 . Correlation between severity of macadamia

decline a nd a mount of root decayed by Kretzschmaria cla-

vus.

4

Botanical Studies, Vol. 50, 2009

1976). At the University of Hawaii Experimental Farm,

a declining macadamia tree with a number of healthy

branches remaining toppled over, without any evidence of

damage from strong winds. Close examination of the tree

revealed that most of the large roots were discolored and

decayed (Figure 2B). Fruiting bodies of Kretzschmaria

clavus (Fr.) Sacc. were found on the surface of the

diseased trunk (Figure 2C) and roots. The same organism

was isolated from decayed tissue and from ascospores

obtained from the stromata of K. clavus. Pathogenicity

tests with this organism demonstrated that the decay

was caused by K. clavus (Ko et al., 1977) (Table 1). The

causal relationship between slow decline and K. clavus

was further supported by the positive correlation between

severity of macadamia decline and the amount of root

decayed by K. clavus (Ko et al., 1977) (Figure 4). In

Taiwan, the majority of macadamia trees showing slow

decline symptoms was caused by Ganoderma lucidum (W.

Curt. Ex Fr.) Karst. Only about 20% of declining trees was

caused by K. clavus (Ann and Ko, 1988).

Quick decline

Members of the investigation committee conducted

a very thorough multidisciplinary field investigation,

and as a result, rainfall, temperature, and other possible

stress factors such as herbicides, fertilization, and tree

crowding and shading were excluded as possible causes

of macadamia quick decline because none of them was

correlated with the incidence of decline (Oi et al., 1991).

Although a number of trees with quick recline symptoms

were infested with ambrosia beetles, they were regarded

as secondary pests attacking weakened trees (Oi et al.,

1991). Exposure of the whole root system of affected trees

also failed to reveal any abnormality of roots like those

observed on trees with slow decline symptoms. Upon

examination of trees at the original site of the quick decline

problem, fruiting bodies of Phellinus gilvus (Schw.) Pat.

(Figure 5A) and Xylaria arbuscula Sacc. (Figure 6A)

were observed on trunks of several trees showing various

stages of decline. These fungi were considered saprobes

and had been ignored previously. Saprobes, by definition,

cannot invade living trees. These trees were still alive.

The presence of fruiting bodies on living trees indicated

that these fungi had potentially established themselves

inside the trunks for a considerable length of time. When

the trunk area with P. gilvus fruiting bodies was cut with

a chainsaw, more than 90% of the cross section surface

was decayed and non-functional (Ko and Kunimoto, 1996)

(Figure 5B), suggesting that P. gilvus was associated with

the decline and impending death of this tree. Ability of

P. gilvus to cause quick decline on macadamia trees was

Figure 5. A, fruiting bodies of Phellinus gilvus produced on

the trunk of a macadam ia tree showing quick decline symp-

toms; B, cross section of diseased trunk showing white rot

caused by the pathogen.

Table 1. Caus al organis m s of s low and quick dec line of

macadamia trees.

Causal organism

Year first reported

(citation)

Reported

as new host

record

Slow decline

Ascomycetes

Kretzschmaria clavus 1977 (Ko et al.)

¡Ï

b

Basidiomycetes

Ganoderma lucidum 1988 (Ann and Ko)

¡Ï

Quick decline

Oomycetes

Phytophthora tropicalis

a

1994 (Ko and Kunimoto) ¡Ð

Ascomycetes

Nectria rugulosa 1991 (Ko and Kunimoto) ¡Ï

Xylaria arbuscula 1991 (Ko and Kunimoto) ¡Ï

Basidiomycetes

Phellinus gilvus

1996 (Ko and Kunimoto) ¡Ï

Hyphomycetes

Acremonium recifei 1999 (Ko and Kunimoto) ¡Ï

a

Originally reported as Phytophthora capsici.

b

¡Ï ¡× yes; ¡Ð ¡× no.

KO ¡X Nature of slow and quick decline of macadamia trees

5

subsequently confirmed by fulfilling Koch¡¦s postulates in

pathogenicity tests (Ko and Kunimoto, 1996) (Table 1).

When the trunk of another declining tree with X. arbuscula

fruiting bodies was cut, it was observed that about 60% of

wood tissue and 100% of bark on the cross section surface

were decayed and non-functional (Ko and Kunimoto,

1991b) (Figure 6B), suggesting that X. arbuscula may be

the cause of decline of this tree. Ability of X. arbuscula

to cause quick decline was later confirmed by completing

Koch¡¦s postulates in subsequent pathogenicity tests (Ko

and Kunimoto, 1991b).

During the subsequent visits to various affected

orchards, fruiting bodies of Nectria rugulosa Pat. were

observed on trunks of many declining macadamia trees

(Figure 7) at several locations on the island of Hawaii and

at one location on the island of Maui (Ko and Kunimoto,

1991a). No visible fungal fruiting bodies were found on

some macadamia trees with quick decline symptoms.

A cross section of the trunk from these declining trees

showed the change of appearance on part of the cut

surface of bark tissue from moist, reddish brown to dry,

grayish brown, and wood tissue from whitish yellow to

grayish (Ko and Kunimoto, 1994; 1999). Isolation of

tissues revealed that the invasion by Acremonium recifei

(Leao & Lobo) Gams or Phytophthora capsici Leonian,

which was subsequently reclassified as Phytophthora

tropicalis Aragaki et Uchida (Aragaki and Uchida, 2001),

had already reached or was about to reach the trunk center

(Ko and Kunimoto, 1999) (Table 2). Pathogenicity tests

also confirmed the ability of each organism to cause quick

decline of macadamia trees (Ko and Kunimoto, 1994;

1999) (Table 1).

Figure 6. A, fruiting bodies of

Xylaria arbuscula produced on trunk

of a m acada mia tree showing quick

decline symptom s. B, cross section of

a diseased trunk showing characteris-

tic black lines.

F ig u re 7. Fruiting bodies of Nectria rugulosa produced on

t runk of a macadam ia t ree showing quick decline symptoms.

Figure 8. Bleeding on the trunk of a macadamia tree show-

ing quick decline symptoms caused by Phytophthora tropica-

lis.

6

Botanical Studies, Vol. 50, 2009

Phytoplasmas were once associated with a quick

decline of macadamia trees (Borth et al., 1994a; 1994b).

However, phytoplasma infection has never been reported

to cause zonal lesions in the wood tissue of trunks (Agrios,

2005) like those observed on declining macadamia trees

(Table 3). Using direct-PCR and ultrasensitive nested-

PCR assays, phytoplasmas were not detected in either

symptomless trees or trees with quick decline symptoms

(Lee and Ko, 1998), thus refuting the suggestion that

phytoplasmas may play a role in macadamia quick

decline. Subsequent tests by others also failed to detect

phytoplasmas in declining macadamia trees (Borth et al.,

1999).

SYMPTOMS AND SIGNS OF SLOW AND

QUICK DECLINE

Refer to Table 3 for a diagnostic key to identify slow

and quick decline and causal organisms.

Slow decline

Slow decline of macadamia trees may be recognized at

a distance by defoliated branches in the canopy of lighter

color (Figure 2A). When affected branches appear on

one side of the canopy, it is an indication of the position

where root decay occurs. The disease progresses very

slowly. More than 10 years after the appearance of

initial symptoms of leaf yellowing on a single branch,

a declining tree will remain alive with only one or two

twigs with green leaves on the lower part of the trunk. K.

clavus produces small, black, mushroom shaped stromata

on large exposed roots and the basal trunk of the affected

tree (Figure 2B). The wood of the diseased roots (Figure

2C) and trunk turns brown, shows distinct black lines

consisting of pigmented hyphae, and remains firm and

hard (Table 3). Ganoderma lucidum produces large brown

basidiocarps with stipe on the lower trunk or on the ground

above decaying roots. It is readily isolated from diseased

trees (Ann and Ko, 1988). The wood near fruiting bodies

turns soft and white (Table 3).

Quick decline

During the early stages of disease development, quick

decline of macadamia trees may be recognized by the

subtle loss of the dark green canopy color and a slight

browning of the whole tree (Figure 3A). The most striking

feature of quick decline is a dark brown tree among normal

green trees during the final stage of disease development

(Figure 3B).

Nectria rugulosa produces small reddish perithecia in

aggregates on the trunk of the affected tree (Figure 7). The

Table 3. Diagnostic key for slow and quick decline of macadamia trees and the causal organisms.

Symptom and Sign

Type of Decline and

Causal Organism

A. Yellowing and browning of leaves on some branches; death of trees takes more than 10 years¡K¡K¡K.....

1.

Small mushroom-shaped carbonaceous stromata (2-5 mm in diameter) on exposed roots and lower

trunk; diseased woody tissue firm with distinct black line¡K¡K¡K¡K¡K¡K.¡K¡K¡K¡K¡K¡K¡K.................

2.

Large brown basidiocarps (4-10 cm in diameter) with stipe on lower trunk and ground above

decaying roots, wood near fruiting bodies soft and white¡K¡K¡K¡K¡K¡K¡K.¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K...

Slow Decline

Kretzschmaria clavus

Ganoderma lucidum

B.

Color of leaves in whole canopy changes from dark green, to light green, to yellow and finally brown;

trees die within 2 to 3 months after leaves turn dark brown¡K¡K¡K¡K¡K¡K¡K¡K¡K..¡K¡K¡K¡K¡K¡K¡K¡K...

1.

Aggregates of small reddish perithecial (0.2-0.4 mm in diameter) on trunk; infected bark dry and

dead, infected wood grayish¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K..¡K¡K

2.

Small club-shaped black perithecial stromata (5-8 ¡Ñ 2-3 mm) on trunk; infected bark dry and dead,

infected wood with distinct black lines¡K¡K......¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K..

3.

Large dark yellowish brown basidiocarps (2-15 cm in diameter) on trunk; bark and wood near

fruiting bodies extensively decayed, whitish and soft¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K¡K..¡K¡K...

4.

Bleeding on trunk; under bleeding area bark blackish brown, wood grayish brown¡K¡K¡K¡K¡K¡K¡K¡K

5.

Neither fruiting bodies nor bleeding on trunk; infected area bark dry and dead, wood light brown¡K...

Quick Decline

Nectria rugulosa

Xylaria arbuscula

Phellinus gilvus

Phytophthora tropicalis

Acremonium recifei

Table 2. Isolation of Nectria rugulosa and Phytophthora

tropicalis from wood at various horizontal distances from the

bark (0 mm) in cross-section of trunks of declining macadamia

trees

Distance from bark (mm)

a

Tissues with pathogen (%)

b

N. rugulosa P. tropicalis

0

63

47

20

73

87

40

56

47

60

54

27

80

37

27

100

37

0

a

Three to ten pieces of wood tiss ues taken at each distance

from a diseas ed tree were tested (Ko and Kunimoto, 1991a;

1994).

b

Data were average of three trees for each pathogen.

KO ¡X Nature of slow and quick decline of macadamia trees

7

bark of the diseased trunk is dry and dead, and the wood

becomes grayish (Table 3). Pathogenicity tests confirmed

this as a pathogen. Small club-shaped black perithecial

stromata are produced on the trunks of declining trees

infected with X. arbuscula (Figure 6). The bark of the

diseased trunk is dry and dead, and the wood turns brown

and shows distinct black lines like those caused by K.

clavus (Table 3). Both X. arbuscula and K. clavus belong

to the black-line producing Xylariaceae (Rogers, 1979).

Phellinus gilvus produces large, dark yellowish-brown

basidiocarps on the trunks of affected trees (Figure 5). The

diseased wood tissue turns brown, and eventually become

white and soft like wood affected by G. lucidum (Table 3).

Both fungi belong to white-rot producing Polyporaceae,

and both have bean confirmed as pathogens. P. tropicalis

causes bleeding on the trunk of a declining tree (Figure 8).

The bark of the diseased trunk becomes blackish brown,

and the wood tissue turns grayish brown (Table 3). Quick

decline caused by A. recifei shows no abnormality on the

trunk surface of affected tree. However, cross-sections of

the diseased trunk display dead dry black to light brown

wood tissue (Table 3). Pathogenicity tests of both P.

tropicalis and A. recifei reproduce these symptoms.

INOCULUM SOURCES AND INITIAL

INFECTION

Slow decline

Most macadamia orchards on the island of Hawaii are

located near forests, and also were originally covered

with forest trees. The predominant tree species prior to

macadamia production were ohia (Metrosideros collina

subsp. polymorpha), melochia (Melochia indica) ,

trumpet tree (Cecropia peltata) and Hawaiian tree fern

(Cibotium glaucum). A survey conducted in the forest near

macadamia orchards revealed the presence of K. clavus

fruiting bodies on dead or diseased trunks of melochia

and trumpet tree. Isolates of K. clavus obtained from these

two tree species were capable of infecting macadamia

trees (Ko et al., 1986). Therefore, diseased tissues and

fruiting bodies incorporated into the soil during the

ground preparation for planting of macadamia trees were

considered the main source of primary inoculum for initial

infection in the new orchard. After establishment of an

infection site on root, the pathogen will begin to colonize

the root system and provide secondary inoculum for initial

infection of roots of adjacent healthy trees through root-

to-root contact (Ann et al., 2002). In the vicinity of Hilo

on the island of Hawaii, ascospores discharged from

fruiting bodies produced on exposed roots and trunk may

be carried by rainwater through the rocky and porous

volcanic soil to reach macadamia roots underground (Ko,

1982) and serve as another source of secondary inoculum

for an initial infection of roots.

Quick decline

Quick decline of macadamia trees results from trunk

infection by various pathogens (Table 3). Infection of

tree trunks by wood-decay organisms is usually through

wounds (Adaskaveg and Ogawa, 1990). On the island

of Hawaii, trunk infection of macadamia trees originates

about 60 cm above the ground (Ko and Kunimoto, 1991a,

1991b, 1996) (Figure 9). The infection site correlates

to injury caused by the mechanical shakers used by

larger growers to remove nuts from the trees, and/or by

flying small, sharp broken lava rocks during the clearing

of leaf debris with leaf blowers. The known inocula

for initial infection include basidiospores of P. gilvus,

ascospores, marconidia and microconidia of N. rugulosa

and X. arbuscula, conidia of A. recifei, and sporangia

and zoospores of P. tropicalis. Oospore production by P.

tropicalis rarely occurs in nature because the organism

is heterothallic (Ko, 1998; 2007). Phellinus gilvus has a

wide host range (Farr et al., 1989; Adaskaveg and Ogawa,

1990). Therefore, fruiting bodies produced on diseased

forest trees or cultivated trees may serve as the source

of basidiospores for initial infection by this pathogen.

The fruiting bodies produced on diseased trunks of

macadamia (Figure 5) may then become the secondary

inoculum source for infection of other macadamia trees.

P. tropicalis also causes raceme blight (Kunimoto et al.,

1976) and foliar blight (Aragaki and Uchida, 1980) in

macadamia. Sporangia produced on diseased racemes and

leaves, therefore, may serve as the main source of primary

inoculum for initial infection. It is not known if the

organism also produces sporangia on diseased trunks. The

sources of primary inoculum of X. arbuscula, N. rugulosa,

and A. recifei are still unknown. The fruiting bodies of X.

arbuscula (Figure 8) and N. rugulosa (Figure 7) produced

on diseased trunks may serve as the sources of inoculum

for infection of other macadamia trees. Whether secondary

inoculum of A. recifei is produced on the surface of

diseased trunks remains to be investigated.

Figu re 9. Area of t runk showing symptom s of infection by

Phellinus gilvus (re d dot) or Xylaria arbuscula (gre en dot)

on cross sections of macadamia trunks cut every 30-40 cm

starting from the soil line.

8

Botanical Studies, Vol. 50, 2009

MODES OF DISEASE DEVELOPMENT

RESULTING IN SLOW AND QUICK DECLINE

Slow decline

The root system of macadamia trees appear to be

slightly resistant to K. clavus as destruction of root by this

pathogen progresses very slowly. When K. clavus infects

the macadamia root system, the affected trees with the

diseased roots appear healthy for several years. It usually

takes more than 5 years to cause approximately 10% root

decay and initiate foliar symptoms on a few branches (Ko

et al., 1977). Root decay reduces the amount of water and

mineral nutrients translocated from soil to leaves. As a

result, affected trees shed many leaves, and as the quantity

of roots decayed increases, the amount of leaves lost also

increases (Figure 4). Because the decay of macadamia

roots caused by K. clavus is relatively slow, usually more

than 10 years are required for the amount of root decay to

reach more than 80%, leading to severe crown dieback and

eventual death of the tree (Ko et al., 1977).

Quick decline

As the pathogen colonizes the woody tissues of the

trunk from the point of infection, the area of decay

expands vertically in both directions and horizontally

across the trunk. Apparently, the diseased trunk continues

to transport water and nutrients, providing an adequate

supply to the entire canopy before the final stage of the

disease development. By the time the first foliar symptoms

of slight browning of the entire canopy of quick decline

are visible, 90 to 100% of the bark and 58 to 97% of

the wood have been killed by the pathogens (Ko and

Kunimito, 1991a; 1991b; 1994; 1996; 1999). Therefore,

before the appearance of visible canopy symptoms, the

pathogen has already been in the bark and wood for an

undetermined period of time without causing a significant

adverse effect on transportation of water and nutrients.

When the majority of the vascular system is blocked by

infection of the pathogen, the onset of the decline resulting

in death of the tree will occur within a relatively short

period of time because a large amount of water is needed

to sustain the whole tree.

Decline caused by multiple infections

Although a single pathogen can cause a slow or quick

decline, depending on the position of initial infection,

infection of a macadamia tree in nature by two different

pathogens has also been observed. Our field survey

revealed the concurrent presence of fruiting bodies of

both N. rugulosa and X. arbuscula on some macadamia

trees with quick decline symptoms (Lee and Ko, 1998).

Isolation from diseased tissues of quick-declining

macadamia trees without visible fungal fruiting bodies

also showed the existence of P. tropicalis and A. recifei on

the same trees at one of the four locations surveyed (Ko

and Kunimoto, 1999). The mode of interaction between

two different pathogens on the same tree remains to be

investigated. If the infections do not occur on the same

side of the trunk, complete girdling and death of affected

trees may occur faster.

DISEASE MANAGEMENT

Because of the severity of the problem, various

fungicides and application methods have been tested

for controlling quick decline of macadamia trees in the

field. However, the results have not been satisfactory.

Ridomil 2E was used as a trunk spray and soil drench, and

Alliette was used as a trunk spray. Trees were treated at

3-month intervals. Although certain treatments appeared

to be effective in slowing the disease progress during the

24-month test period, browning of leaves and eventual

death of trees inevitably followed. Similar results were

obtained when Kocide and a systemic experimental

fungicide, WECO-42894, were applied as a trunk spray.

Injection of macadamia trees with Alliette also slowed the

death of trees for about 6 months, but by the 7th month

there was no difference in tree death between injected and

control trees (Wayne Nishijima, personal communication).

Currently, no resistant cultivars are available for control

of slow or quick decline of macadamia. Recommended

measures for disease management include removal of

diseased plants and orchard cultivation practices that

minimize tree wounding. Because of the presence of K.

clavus fruiting bodies on the dead and diseased trunks

of trees in the forest (Ko and Kunimoto, 1986), the stem

tissue of forest trees should be removed during the land

preparation for new plantings of macadamia. Macadamia

trees in the orchards infected with K. clavus should be

removed along with major roots. The surrounding area of

macadamia orchards should be free of dead tree branches

to avoid their colonization by K. clavus and production of

fruiting bodies on colonized branches (Ko, 1979) that may

serve as an inoculum source.

Racemes and leaves infected with P. tropicalis should

be cut and removed to reduce the primary inoculum of this

pathogen. Trunks of trees with quick decline symptoms

should be destroyed by burning to prevent spread of the

disease in the orchards by secondary inocula. Cultural

practices, including mechanical harvesting and leaf dearing

and chemical and mechanical methods of weed control,

which may cause wounds on trees, should be performed

with great caution to minimize injury to trunks.

CURRENT STATUS AND FUTURE

OUTLOOK

Besides Hawaii, slow decline of macadamia trees also

has been reported from Taiwan (Ann and Ko, 1988). More

reports concerning the incidence of macadamia slow

decline induced by fungal root rot may come from other

countries in the future. Quick decline of macadamia is

not expected to be severe in other macadamia-growing

countries, unless a significant amount of trunk damage

KO ¡X Nature of slow and quick decline of macadamia trees

9

occurs as the result of inappropriate cultural practices.

A rapid method for screening macadamia seedlings

for resistance to K. clavus was developed in 1986 (Ko

and Kunimoto, 1986). However, a selective breeding and

screening program has not been implemented since then

due to lack of funds. In the future with funds available

cultivars resistant to K. clavus may be obtained through

a selection program and used as the root stock for control

of slow decline. Commercial cultivars of macadamia have

been shown to differ in susceptibility to A. recifei (Ko and

Kunimoto, 1999). All commercial cultivars of macadamia

should be tested for susceptibility to all known pathogens

associated with quick decline and trees with quick decline

symptoms should be diagnosed to determine the causal

agent. Extension agents can use this information to advise

growers on selection of cultivars for replanting in affected

orchards.

Fungicides should also be tested for ability to prevent

wounded trunks from infection by the known quick

decline pathogens. Effective fungicides can then be tested

in the field to determine the feasibility of applying these

chemicals to a vulnerable area of the trunk following each

harmful cultural practice. Development of soil drenches

or soil fumigation prior to replanting to reduce the decline

incidence is also urgently needed.

Acknowledgments. The author thanks Jyh-Nong Tsai

and Hsiu-Fang Cheng for preparation of figures, and

the National Science Council of Taiwan for its financial

support (NSC 97-2321-B-005-007-MY3).

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Botanical Studies, Vol. 50, 2009