Scientia Horticulturae 150 (2013) 354–359

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Scientia Horticulturae
journal homepage: www.elsevier.com/locate/scihorti

Review

The reproductive biology of macadamia

Stephen J. Trueman ∗
University of the Sunshine Coast, Maroochydore, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Macadamia is a widely-grown tree crop that produces edible kernels with high oil content. The
Received 10 October 2012 macadamia kernel is the single embryo of the fruit, and so factors that influence fruit set and embryo
Accepted 27 November 2012 development are critical regulators of yield and quality. This review summarises over 75 years of research
on floral induction, floral structure, pollen transfer, the breeding system and fruit development of
Keywords: macadamia, highlighting features such as insect pollination and partial self-incompatibility that limit
Flowering
orchard productivity and affect kernel quality.
Kernel
© 2012 Elsevier B.V. All rights reserved.
Nut
Pollination
Proteaceae
Self-incompatibility

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354
2. Floral induction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 355
3. Floral structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 355
4. Pollen transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356
5. Breeding system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356
6. Fruit development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 357
7. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 357
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 357

1. Introduction et al., 1995). Macadamia is grown extensively in commercial plan-

tations in Australia, South Africa, Brazil, Hawaii, Kenya and Costa
The genus, Macadamia (Proteaceae), is comprised of four ever- Rica, and most cultivars have been derived from selection pro-
green tree species endemic to the rainforests and rainforest fringes grammes in Hawaii and Australia that identified superior-yielding
of subtropical eastern Australia (Mast et al., 2008; Neal et al., 2010; seedling trees (Nagao and Hirae, 1992; Stephenson and Gallagher,
Shapcott and Powell, 2011). The kernels of two species, M. jansenii 2000; Peace et al., 2003; Steiger et al., 2003; Hardner et al., 2009).
and M. ternifolia, are inedible due to the presence of high levels These cultivars are propagated clonally by grafting onto seedling
of cyanogenic glycosides, and so macadamia cultivars are derived rootstocks, although tissue culture methods have been developed
from two freely-hybridising species, M. integrifolia and M. tetra- recently for macadamia seedlings (Cha-um et al., 2011). Orchards
phylla, that contain low levels of cyanogenic glycosides in their are typically comprised of two or more cultivars, often with a
mature kernels (Storey, 1985; Gross and Weston, 1992; Dahler principal cultivar and the other cultivars planted in ‘pollinator’
rows. However, macadamia is sometimes planted in partial or com-
plete blocks of a single cultivar (Ito and Hamilton, 1980; Stace,
1986; Trueman et al., 2002). The commercial product of macadamia
∗ Correspondence address: Faculty of Science, Health, Education and Engineering,
is the single embryo of the fruit, and so limitations to fruit set
University of the Sunshine Coast, Maroochydore, DC 4558, Australia.
and embryo development have important economic consequences
Tel.: +61 7 5456 5033. for macadamia growers. This review describes the processes of
E-mail address: strueman@usc.edu.au floral initiation, flowering, pollination and fruit development in

0304-4238/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.scienta.2012.11.032
 S.J. Trueman / Scientia Horticulturae 150 (2013) 354–359
Fig. 1. (a) Macadamia racemes progressing from pre-anthesis (left raceme) to anthesis (right raceme). Scale bar = 30 mm; (b) raceme in which most flowers have opened. A
small stingless bee (Tetragonula sp.) is foraging at flowers near the top of the raceme. Scale bar = 15 mm; (c) A macadamia infructescence at the stage of immature fruit drop.
Scale bar = 10 mm.
macadamia, focussing on factors that might limit fruit set, nut yield
and kernel quality.
2. Floral induction
Macadamia has three buds in every leaf axil that can poten-
tially develop into shoots or inflorescences (Storey, 1985; Wilkie
et al., 2009a). Usually only one of the buds develops in each leaf
axil and, since there are three leaves per node in M. integrifolia
and four leaves per node in M. tetraphylla, three or four inflore-
scences develop per node in these species and their hybrids (Storey,
1985). The inflorescence is a pendant raceme (Fig. 1a) bearing
between 100 and 300 flowers, with whorls of six pairs of flowers
at each node of the rachis (Storey, 1985; Joubert, 1986; Trueman
and Turnbull, 1994a). Floral initiation in the orchards of eastern
Australia occurs during late autumn or winter when minimum tem-
peratures are between 11 ◦ C and 15 ◦ C (Moncur et al., 1985; Olesen,
2005; Wilkie et al., 2010). Macadamia buds undergo little growth
for 50–96 d after initiation (Moncur et al., 1985) possibly because of
unfavourable environmental conditions such as cool temperature
and low solar irradiance (Moncur et al., 1983). Raceme elonga-
tion commences in mid-late winter (Moncur et al., 1985) and peak
anthesis usually occurs in late winter or early spring (Heard, 1993;
Nagao et al., 1994; Trueman and Turnbull, 1994a,b; Wallace et al.,
1996; Wilkie et al., 2009a).
The effects of photoperiod on floral initiation in macadamia are
not known, although macadamia may be day-neutral as M. integri-
folia produces flowers all the way from the Equator to 40◦ S. Floral
initiation of potted trees at a controlled day temperature of 25 ◦ C
occurs at a wide range of night temperatures (5 ◦ C, 10 ◦ C, 15 ◦ C and
20 ◦ C) although raceme production during a return to low ambi-
ent temperatures (mean 10.5 ◦ C at night) is much greater in trees
that have been exposed to the warmest (20 ◦ C) nights (Stephenson
and Gallagher, 1986). However, in trees that have already initiated
floral buds, further raceme production occurs at night tempera-
tures of 12 ◦ C, 15 ◦ C and 18 ◦ C but it is almost completely inhibited
at 21 ◦ C (Nakata, 1976). Removal of an entire season’s racemes
can invoke an earlier and more intense flowering in the follow-
ing season (Stephenson et al., 1989), trunk girdling before floral
buds become visible can almost double the number of racemes pro-
duced in that season (Nagao and Sakai, 1990), and application of
the growth retardant, uniconazole, greatly increases flowering of
young trees (Nagao et al., 1999). These results suggest that carbo-
hydrate availability may also affect floral initiation.
355
Mature macadamia trees can produce up to 2500 racemes in a
flowering season (Moncur et al., 1985; Moncur, 1988; McFadyen
et al., 2011; Olesen et al., 2011). In many cultivars, some racemes
are produced on stems less than 1 year old, but most are produced
on wood at least 2 years old in areas of the canopy that are heavily
shaded (Nagao et al., 1994; Wilkie et al., 2009a; Olesen et al., 2011).
However, some cultivars such as A4 produce many racemes on
young stems at the outer edge of the canopy (Wilkie et al., 2009a).
Racemes tend to be produced on less-vigorous and shorter stems;
e.g. <30-cm length in cultivar 660, <60-cm length in cultivars A38
and 695, and <80-cm length in cv. A4 (Wilkie et al., 2009a).
Canopy pruning is required to allow machinery access and
improve spray penetration in macadamia orchards (McFadyen
et al., 2004, 2005). Yield can be strongly affected by the timing of
canopy pruning because pruning disturbs the cycle of recurrent
vegetative flushes, subjecting the new flush to different conditions
of temperature and irradiance and altering carbohydrate availabil-
ity (Olesen et al., 2006; Wilkie et al., 2009b, 2010). This, in turn,
affects stem elongation, raceme production and abscission of the
young fruit (Olesen, 2005; Wilkie et al., 2009b, 2010; Olesen et al.,
2011; McFadyen et al., 2011, 2012a,b). Pruning times, such as early
autumn, that provide an immature vegetative flush in late autumn
and early winter can inhibit raceme production and reduce yield
(Wilkie et al., 2010). Other pruning times, such as early to mid-
spring, that provide an immature vegetative flush during early fruit
development can increase abscission of young fruit and also reduce
yield (McFadyen et al., 2011, 2012a).
3. Floral structure
Macadamia flowers at anthesis are typically about 15 mm
long including a 3-mm pedicel, with one anther attached by
a short filament to each of four petal-like perianth segments
(Scholefield, 1982; Storey, 1985; Joubert, 1986). The pistil consists
of a unicarpellate, superior, pubescent ovary and a slender style
with a club-shaped tip, on which rests the small stigmatic area
(Urata, 1954; Storey, 1985; Wallace et al., 1992). The ovary con-
tains two orthotropous ovules (Sedgley, 1981; Strohschen, 1986).
Macadamia styles begin to elongate and bend about 6–7 d before
anthesis, and the mid-portion of the style protrudes through the
abaxial suture between two perianth segments 2–5 d before anthe-
sis (Urata, 1954; Sedgley et al., 1985). Anther dehiscence occurs
1–2 d before anthesis (Urata, 1954; Sedgley et al., 1985) and the tri-
aperturate pollen is deposited in clumps on the stigma and upper
356 S.J. Trueman / Scientia Horticulturae 150 (2013) 354–359
style (Sedgley et al., 1985; Wallace et al., 1992), where it may be
brushed by foragers. Anthesis often progresses basipetally along
racemes (Urata, 1954; Pisanu et al., 2009) but it may also progress
acropetally, from the centre, or from both ends depending on the
cultivar and environmental conditions.
Pollen presentation on the upper style and stigma may seem
to be an adaptation for self-pollination but many species of
the macadamia family, Proteaceae, also exhibit protandry and
self-incompatibility (Ladd, 1994; Goldingay and Carthew, 1998;
Matthews and Sedgley, 1998; Collins et al., 2008). Much of
the self-pollen may be removed, and other pollen deposited,
before the stigma becomes receptive (Ladd, 1994; Goldingay
and Carthew, 1998). In macadamia, pollen germination does
not occur until 1–2 d after anthesis, coincident with the devel-
opment of an extracellular secretion on the stigma papillae
(Sedgley et al., 1985; Wallace et al., 1992). Pollen collected from
a flower at 1 d before anthesis, however, will germinate on the
stigma of a 3-d post-anthesis flower, indicating that the pollen
is mature before anthesis but that the stigma is still unreceptive
(Sedgley et al., 1985).
4. Pollen transfer
Pollen is transferred in macadamia orchards predominantly by
insects. A range of insect visitors has been observed on macadamia
racemes in Hawaii, with the most common being honeybees and, to
a lesser extent, syrphid flies (Urata, 1954). No birds were observed
foraging at macadamia racemes. Specimens of both honeybees and
syrphid flies were covered in macadamia pollen, and pollen pellets
trapped at the entrances to honeybee hives indicated that some
hives had a preference for macadamia pollen. Pollen-collecting
honeybees were adept at removing pollen clumps from the upper
style, and fruit sets at 15–20 d after anthesis were higher on open-
pollinated racemes than on racemes that were bagged to exclude
insect visitors. Vaseline-coated glass slides were placed in the
orchard to assess the possibility of wind-pollination, but wind was
found to be of only minor importance for effecting macadamia pol-
lination (Urata, 1954).
Honeybees and the native stingless bee, Tetragonula spp. (for-
merly Trigona spp.) (Fig. 1b), are the most abundant floral visitors
in Australian macadamia orchards, although a wide range of other
insects and some birds have also been observed (Vithanage and
Ironside, 1986; Heard, 1994; Heard and Exley, 1994; Wallace et al.,
1996; Blanche et al., 2006). The foraging behaviour of honeybees
and stingless bees, and particularly their pollen-collecting work-
ers, ensures that contact is made with the stigma (Vithanage and
Ironside, 1986; Heard, 1994), and workers carry large numbers of
pollen grains (Vithanage and Ironside, 1986). Bagging of racemes
to exclude insect visitors greatly reduces the percentage of flowers
with a pollen tube at the base of the style (Vithanage and Ironside,
1986) and also reduces final fruit sets (Heard, 1993, 1994; Wallace
et al., 1996). No fruit is formed if racemes are bagged during the
day, but not at night, indicating that nocturnal foragers do not pol-
linate macadamia in Australian orchards (Vithanage and Ironside,
1986; Heard, 1993).
5. Breeding system
Macadamia is partially self-incompatible, with more flowers
exhibiting pollen tube penetration to the lower half of the style
following cross-pollination than self-pollination (Sedgley, 1983;
Sedgley et al., 1990). Arrest of pollen tube growth occurs in
the upper style, with inhibited tubes having swollen tips and
apparently discharging their contents through a sub-terminal pore
(Sedgley, 1983; Sedgley et al., 1985). Initial fruit sets, assessed when
swelling of the ovary becomes apparent at 7–21 d post-pollination,
also suggest that macadamia is partially self-incompatible (Urata,
1954; Ito and Hamilton, 1969; Ito et al., 1970, 1983; Sedgley et al.,
1990). These reports did not present final fruit sets although Urata
(1954) provided some data from 45 to 70 d after pollination, when
abscission of immature fruits (Fig. 1c) would have been near com-
pletion (Sakai and Nagao, 1985; Trueman and Turnbull, 1994b;
McFadyen et al., 2011, 2012b). Final fruit set in wild popula-
tions of M. tetraphylla is much greater following cross-pollination
(3.25–6.79%) than self-pollination (0.67%), confirming partial self-
incompatibility in this species (Pisanu et al., 2009).
The presence of a partial self-incompatibility system, deter-
mined from controlled self- and cross-pollination treatments, does
not indicate that final fruit set is necessarily limited by the amount
of available cross-pollen. Other factors such as resource limita-
tion, predation or disease may determine the achievable levels
of fruit set in a particular situation (Stephenson, 1981; Ayre
and Whelan, 1989; Trueman and Wallace, 1999; Wallace et al.,
2002a,b). The importance of pollen source and pollen limitation
as determinants of fruit set can be tested by supplementing the
naturally-deposited pollen with added cross-pollen (Bartomeus
and Vilà, 2009; González-Varo and Traveset, 2010). Supplementary
cross-pollination of macadamia increases the percentage of flowers
with a pollen tube in the lower style (Trueman and Turnbull, 1994a)
and increases fruit set at 14 or 21 d after pollination (Trueman and
Turnbull, 1994a; Wallace et al., 1996). These increases in pollen
tube penetration and initial fruit set often translate into higher final
fruit set. Supplementary cross-pollination increased final set by 57%
and 97% in two experiments with cultivar 246 and by 64% and 95%
in two experiments with cultivar 660, whereas final set was unaf-
fected in two experiments with cultivar A4 and one experiment
with each of cultivars 333 and 660 (Trueman and Turnbull, 1994a;
Wallace et al., 1996). Kernel weights were measured in four of
these experiments, with supplementary cross-pollination increas-
ing weights by 18% in cultivar A4, by 20% in cultivar 246, and by
24% and 31% in cultivar 660 (Trueman and Turnbull, 1994a; Wallace
et al., 1996).
Paternity analysis of kernels from a pure block of 27 rows of
cultivar A16 trees, flanked by cultivars 344 and 741 on one side
and cultivar A4 on the other, has found surprisingly-low levels of
self-pollination even at 14 rows (98 metres) from the pollinator
cultivars (Vithanage et al., 2002). Approximately 85–90% of kernels
in the centre of the pure block were the result of cross-pollination,
similar to the levels found (81–100%) in rows near the pollinator
cultivars. However, yields were approximately 20–42% lower in the
centre of the block than in the rows near the most effective pollina-
tor, cultivar A4. This demonstrates that the realised mating system
of cultivated macadamia is predominantly outcrossing, that yield
is limited by the flow of cross-pollen across the orchard, and that
high yield cannot be achieved through self-pollination.
The need for insects to transfer cross-pollen of macadamia
means that growers must consider their orchard design, pollinator
management and pesticide application strategies to ensure high
yield and kernel quality (Wallace et al., 1996). The availability of
cross-pollen could be improved by closer inter-planting of different
cultivars, because insect-mediated pollen flow in orchards is some-
times confined to neighbouring rows of trees (Wallace et al., 1996,
2002a, b; Vezvaei and Jackson, 1997; Soejima, 2007). Bee hives
can be introduced into orchards to increase pollinator populations.
Honeybee hives have been placed in macadamia orchards for many
years (Urata, 1954; Shigeura et al., 1970; Gary et al., 1972; Stock,
1979; Stace, 1986; Heard, 1999) and some growers in Australia have
recently been introducing stingless bee hives. Pesticide application
during macadamia flowering is usually avoided or, at most, prac-
tised only in the early evening to prevent bee mortality and allow
maximal pollination.
 S.J. Trueman / Scientia Horticulturae 150 (2013) 354–359 357

6. Fruit development

Fertilization occurs within 1 week of anthesis (Ito, 1980;

Sedgley, 1983) and normally only one of the two ovules is fertil-
ized (Sedgley, 1981; Trueman and Turnbull, 1994a). Most flowers
abscise during the following 2 weeks (Sakai and Nagao, 1985;
Trueman and Turnbull, 1994a,b; Wallace et al., 1996; McFadyen
et al., 2011, 2012a,b). Free nuclear endosperm develops rapidly
in the remaining fruits for several weeks before cell walls are
laid down around 8–11 weeks after anthesis (Hartung and Storey,
1939; Strohschen, 1986). Endosperm development coincides with a
period of high cytokinin accumulation, but low gibberellin levels, in
the fruit (Trueman, 2010a, 2011), and final fruit set is not affected by
applications of cytokinin, gibberellin, auxin, or the ethylene synthe-
sis inhibitor, aminoethoxyvinylglycine (Williams, 1980; Trueman,
2010b; McFadyen et al., 2012b). Embryo development occurs more
gradually than endosperm development, but the cotyledons com-
pletely replace the cellular endosperm by 20 weeks after anthesis
(Hartung and Storey, 1939; Strohschen, 1986). Immature fruit drop
occurs during the first 7–15 weeks after anthesis, with the timing of
this fruit drop depending on the site, cultivar, and time since canopy
pruning (Sakai and Nagao, 1985; Trueman and Turnbull, 1994b;
Trueman, 2010b; McFadyen et al., 2011, 2012a). Retention of imma-
ture fruit is strongly related to available carbohydrate levels, and
this phase of fruit drop might represent a maternal adjustment of
crop load prior to the major period of fruit biomass accumulation
(Trueman and Turnbull, 1994b; McFadyen et al., 2011, 2012a).
Macadamia fruit increase in diameter up to 15–16 weeks after
anthesis (Sakai and Nagao, 1985; Trueman and Turnbull, 1994b),
but most biomass accumulation occurs between 13 and 24 weeks
after anthesis when the shell hardens and the kernel accrues oil
(Jones, 1937, 1939; Jones and Shaw, 1943; Nagao and Sakai, 1988;
Trueman and Turnbull, 1994b). Mature kernels contain approxi- Fig. 2. (a) Macadamia fruit (nut-in-husk) showing progressive dehiscence of the
pericarp (the husk) to reveal the testa (the shell). (b) Macadamia seed (nut-in-shell,
mately 66–82% oil (Mason and Wills, 1983; Trueman et al., 2000).
on left) and embryo (the kernel, on right). Two kernels are ‘wholes’ and two kernels
The fruits of some cultivars such as 344 and 741 abscise soon after have separated between the cotyledons to form ‘halves’. Scale bars = 25 mm.
oil accumulation, while the fruits of other cultivars such as A16 and
246 remain on the tree for several months before abscission (Nagao
and Sakai, 1988; Trueman et al., 2000, 2002). therefore, critical for maximising the quality of kernels (Walton
The fruit is a follicle (Hartung and Storey, 1939; Johnson and Wallace, 2008, 2009, 2010, 2011; Le Lagadec, 2009).
and Briggs, 1975; Strohschen, 1986), consisting of a dehiscent
pericarp (the husk) which encloses the lignified testa (the shell) 7. Conclusions
and the embryo (the kernel) (Fig. 2). Fruits are harvested from the
orchard floor usually after natural abscission, although fruit drop Macadamia is an annual-flowering, evergreen tree that is
is sometimes induced by the ethylene-generating compound, (2- bee-pollinated, partially self-incompatible and predominantly out-
chloroethyl)phosphonic acid, or by the use of mechanical shakers crossing. Achieving high nut yield and kernel quality is dependent
(Trochoulias, 1986; Stephenson and Gallagher, 1987; Nagao and upon understanding the tree’s vegetative and reproductive cycles
Hirae, 1992; Richardson and Dawson, 1993; Trueman et al., 2002; to ensure heavy flowering, active pollinator populations, deposition
Trueman, 2003a,b). The harvested fruits (Fig. 2a) are dehusked of cross-pollen onto stigmas, and high carbohydrate availability
to provide the nut-in-shell (Fig. 2b) and then cracked to provide during early fruit development. Poor flowering and poor retention
the kernel (Walton and Wallace, 2008). The kernels of some of immature fruit can both reduce yield, and so canopy pruning
cultivars such as 344 and 741 are prone to separating between must be timed to prevent a strong flush of immature foliage dur-
the cotyledons to provide ‘halves’, while other cultivars such as ing the periods of floral initiation in late autumn and early winter
A16, A38 and 835 provide a high proportion of ‘whole’ kernels and immature fruit drop in spring. Cross-pollination increases fruit
(Walton and Wallace, 2005a, 2012; Walton et al., 2012) (Fig. 2b). retention, nut yield and kernel size, and so close inter-planting
Susceptibility to breakage appears to be related to the thinness of of different cultivars and the introduction of bee hives are two
the cotyledonary cuticle at the separation zone, the presence of strategies to maximise the transfer of pollen between cultivars and
convolutions in the cuticle, and the width of air spaces between maximise orchard productivity.
the two cuticles (Walton and Wallace, 2005a; Walton et al., 2012).
Kernel breakage and kernel damage can potentially occur during
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