American Journal of Botany 86(9): 12171225. 1999.

COMPARATIVE

MORPHOLOGY AND PHYSIOLOGY OF

FRUIT AND SEED DEVELOPMENT IN THE TWO SHRUBS

RHUS AROMATICA

AND

R. GLABRA (ANACARDIACEAE)1

XIAOJIE LI,2 JERRY M. BASKIN,2,3

AND

CAROL C. BASKIN2,4

School of Biological Sciences, University of Kentucky, Lexington, Kentucky 40506-0225; and 4Department of
Agronomy, University of Kentucky, Lexington, Kentucky 40546-0091

Morphology and physiology of fruit and seed development were compared in Rhus aromatica and R. glabra (Anacardiaceae), both of which produce drupes with water-impermeable endocarps. Phenology of flowering/fruiting of the two species
at the study site was separated by ;2 mo. However, they were similar in the timetable and pattern of fruit and seed
development; it took ;2 mo and ;1.5 mo for flowers of Rhus aromatica and R. glabra, respectively, to develop into mature
drupes. The single sigmoidal growth curve for increase in fruit size and in dry mass of these two species differs from the
double-sigmoidal one described for typical commercial drupes such as peach and plum. Order of attainment of maximum
size was fruit and endocarp (same time), seed coat, and embryo. By the time fruits turned red, the embryo had reached full
size and become germinable; moisture content of seed plus endocarp had decreased to ;40%. The endocarp was the last
fruit component to reach physiological maturity, which coincided with development of its impermeability and a seed plus
endocarp moisture content of ,10%. At this time, ;50, 37, and 13% of the dry mass of the drupe was allocated to the
exocarp plus mesocarp unit, endocarp, and seed, respectively. The time course of fruit and seed development in these two
species is much faster than that reported for other Anacardiaceae, including Rhus lancea, Protorhus, and Pistacia.
Key words: Anacardiaceae; embryo germinability; endocarp impermeability; fruit development; mass allocation to fruit
components; Rhus aromatica; Rhus glabra; seed development.

Development of fruits of economically important species has long been of interest to botanists and plant physiologists (see reviews by Hulme, 1970, 1971; Coombe,
1976). Among the species that have received considerable attention are those with drupaceous fruits such as
peach (Connors, 1919; Lilleland, 1932; Lott, 1932), cherry (Tukey, 1934), plum (Lilleland, 1934), and apricot
(Lilleland, 1930). In these species, the endocarp is stony,
but permeable to water, and the mesocarp is fleshy.
Growth studies also have been done on drupes such as
almond (Brooks, 1939) and hackberry (Cowan et al.,
1997), in which the water-permeable endocarp is surrounded by a nonfleshy mesocarp. However, aside from
studies on developmental anatomy in some species of
Anacardiaceae native to southern Africa (von Teichman,
1987, 1991b, 1993; von Teichman and Robbertse, 1986a,
b), little is known about fruit development in species with
a water-impermeable endocarp.
Further, the relationship between attainment of embryo
germinability and onset of endocarp impermeability has
not been investigated. The impermeable endocarp of the
germination unit (seed plus endocarp) of Anacardiaceae
serves the same function as does the macrosclereid layer
in the seed coat of hardseeded species of Convolvulaceae,
Geraniaceae, Leguminosae, Malvaceae, and other plant
families (Rolston, 1978; Baskin and Baskin, 1998). That
is, the impermeable endocarp prevents water uptake by
1 Manuscript received 11 May 1998; revision accepted 5 February
1999.
The authors thank the personnel at Raven Run Nature Sanctuary,
Fayette County, Kentucky, for allowing them to use the study site and
for facilitating the field work.
2 Author for correspondence.

the embryo and, thus, is responsible for physical dormancy.

Rhus aromatica Ait. and R. glabra L. (Anacardiaceae)
are dioecious shrubs with drupaceous fruits, in which the
endocarp is impermeable to water at fruit maturity and is
the only cause of physical dormancy (Heit, 1967; Farmer,
Lockley, and Cunningham, 1982; Li et al., unpublished
data). Rhus aromatica, the type species of subgenus Lobadium (Young, 1975), mostly is distributed naturally in
eastern United States and adjacent Canada, whereas R.
glabra, of subgenus Rhus, occurs throughout the conterminous United States, north to southern Canada and
south to northern Mexico (Barkley, 1937; Little, 1977).
Rhus aromatica flowers in mid-spring and fruits in early
summer, whereas R. glabra flowers in early summer and
fruits in late summer. The variety of Rhus aromatica at
our study site was Rhus aromatica var. aromatica (Gleason and Cronquist, 1991).
Although there have been quite a few studies on the
biology of some Rhus species (e.g., Boyd, 1943, 1944;
Brinkman, 1974; Farmer, Lockley, and Cunningham,
1982; Lovett Doust and Lovett Doust, 1988; Facelli,
1993), including three dissertations (Gilbert, 1959; Lovell, 1964; Smith, 1970), virtually nothing is known about
the pattern of fruit and seed development for any of the
North American taxa. Thus, as part of a study on the
comparative seed biology of R. aromatica and R. glabra
we investigated the morphological and physiological
changes that take place during fruit and seed development. More specifically, our primary objectives were to
compare the (1) time course and pattern of fruit growth
(size and mass) and of partitioning of dry mass to its
components, and (2) time course of moisture content in
relation to the development of endocarp impermeability
and embryo germinability.

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the latter becomes desiccated. The endocarp is the stony inner part of
the pericarp that encloses the seed. Between the exocarp and endocarp
is the mesocarp, which easily can be detached from the endocarp and
is united permanently with the exocarp in R. glabra. However, the mesocarp in R. aromatica is rather sticky and thus clings to the endocarp,
and is separated spatially from the exocarp. In this study, the exocarp
and mesocarp together are called pulp.

Fig. 1. Monthly precipitation (a) and mean maximum and minimum

temperatures (b) at the study site in 1996 () and 1997 ().

MATERIALS AND METHODS

Study siteThe study site is located in Raven Run Nature Sanctuary
(378539 N and 848239 W), Fayette County, Kentucky, USA, ;20 km
southeast of Lexington. Vegetation at the study site is the herb-shrub
stage of old-field succession (Campbell, Ruch, and Meijer, 1995). The
soil is McAfee silty clay loam, 612% slopes, eroded phase (subgroup
5 Mollic Hapludalfs) (Sims et al., 1968), and bedrock is Lexington
Limestone (Middle Ordovician) (Black, 1967). Mean annual precipitation (most of which is rainfall) at Lexington is 1141 mm and is fairly
evenly distributed throughout the year. Mean annual temperature is
12.88C, with a mean temperature of 0.88C for the coldest month (January) and 24.48C for the hottest month (July) (Hill, 1976). Mean monthly maximum and minimum temperatures and precipitation recorded at
Raven Run during the study period (19961997) are shown in Fig. 1.
22 m2) of R. aromatica and three clumps (X
60
Nine clumps (X
2
m ) of R. glabra plants were used in the study; clumps were separated
by distances of 316 m, and each presumably was a distinct genotype.
Study systemFruits of R. aromatica and of R. glabra are drupes
;7.5 3 6.9 mm and 5.4 3 4.8 mm, respectively. A longitudinal section
of a Rhus aromatica fruit at maturity prior to desiccation is shown in
Fig. 2. A functional approach (von Teichman, 1989, 1991b) is employed
to define the various components of the pericarp. As such, the exocarp
is the papery, relatively thin part of the pericarp in R. aromatica and
in R. glabra that can be detached easily from the rest of the fruit, once

Fig. 2.

Data collectionGeneral morphology of mature female flower, fruit,

and seedAt anthesis, 50 female flowers each of R. aromatica and R.
glabra were collected randomly from the clumps at the study site. The
length and width of flower and length of ovary for each of them were
measured to the nearest 0.01 mm under a dissecting microscope. Color
of the petals (flower color) was noted.
Fifty fruits of each of the two species were collected randomly from
the various clumps at maturity prior to desiccation, and their lengths
and widths measured to the nearest 0.01 mm. Then, the pulp was removed from the fruit manually, and the lengths and widths of the endocarp, seed coat, and cotyledons were measured. Colors of these various fruit components also were recorded.
Time course and pattern of growth in length and widthBeginning
at anthesis, lengths and widths of 50 flowers/fruits and of fruit components (endocarp, seed coat, and cotyledons) each of R. aromatica and
R. glabra were collected weekly during the 1996 and 1997 growing
seasons and measured to the nearest 0.01 mm under a dissecting microscope. On each collection date, five to seven infructescences were
collected from each clump of each species. Flowers/fruits were removed
from all infructescences and pooled. At the beginning (anthesis) and at
the end of fruit development, there was only one size class. Fifty flowers/fruits were chosen randomly from the pool. Between anthesis and
fruit maturity, fruits from all infructescences were pooled and sorted
into four size classes. Fifty fruits were chosen randomly from the size
class with the highest number of fruits. Fruits used in the following
studies also were chosen using this procedure.
Time course and pattern of increase in dry massMasses (fresh and
dry) also were determined for whole fruit, seed plus endocarp, and seed
of R. aromatica and of R. glabra for each collection date. There were
ten replications of ten fruits or of ten component units, i.e., each replicate consisted of ten whole fruits, ten seed plus endocarp units, or ten
seeds. Mass data for pulp and endocarp were derived as follows:
pulp 5 (whole fruit) 2 (seed plus endocarp)

Longitudinal section of a mature Rhus aromatica fruit.

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TABLE 1. General morphology of the maturea female flower, fruit, and

seed of Rhus aromatica and R. glabra.
Trait

R. aromatica

Flower color
Flower length (mm)
Flower width (mm)
Ovary length (mm)
Fruit shape
Fruit ripe color
Fruit length (mm)
Fruit width (mm)
Fruit dry mass (mg)
Endocarp color
Endocarp length (mm)
Endocarp width (mm)
Seed coatb color
Seed coat length (mm)
Seed coat width (mm)
Cotyledon color
Cotyledon length (mm)
Cotyledon width (mm)

Yellowish
2.05 6 0.02
1.90 6 0.01
0.74 6 0.02
Rounded
Bright red
7.52 6 0.06
6.69 6 0.08
40.91 6 0.87
Dark brown
6.27 6 0.06
5.30 6 0.03
Pale creamy
4.90 6 0.09
3.52 6 0.07
Creamy
4.63 6 0.06
3.09 6 0.06

Greenish
2.97 6 0.04
3.38 6 0.07
0.73 6 0.02
Flattened
Dark red
5.44 6 0.04
4.84 6 0.04
14.33 6 0.22
Grey
4.04 6 0.03
3.34 6 0.02
Pale creamy
3.25 6 0.04
2.34 6 0.04
Creamy
2.83 6 0.03
1.60 6 0.02

Mature flowers 5 anthesis. Mature fruits/seeds 5 the time when

fruits first turned red, but were not desiccated.
b Except the dark saddle-like patch.

endocarp 5 (seed plus endocarp) 2 seed.

Dry mass was determined by oven-drying the materials at ;908C until
constant mass was reached (usually ;3 d). All masses were determined
to the nearest 0.01 mg and converted to mass per fruit, per seed plus
endocarp unit, or per seed, prior to statistical analysis.
Time course and pattern of moisture content during development
Data collected in the mass growth study were used for calculating percentage moisture content (%MC), as shown below:
(fresh mass 2 dry mass)
3 100.
fresh mass

Development of embryo germinabilityTo determine when the embryo acquires the ability to germinate, four replicates of 15 embryos
for each collection date were excised, placed on wet sand in petri dishes,
and incubated under ambient laboratory temperature (;228238C) and
light (cool-white flourescent for 1012 h/d) conditions for 7 d, at which
time the percentage of embryos that had germinated (i.e., radicle $ 2
mm) was determined.
Development of endocarp impermeabilityTime of onset of impermeability of the endocarp to water also was determined. The pulp (exocarp plus mesocarp) was manually removed from the fruit, and ten
replications of 20 seed plus endocarp units each were kept on wet sand
in petri dishes under ambient temperature and light conditions for 7 d.
The percentage of seed plus endocarp units that had imbibed water was
determined. An imbibed seed plus endocarp unit easily can be distinguished visually from a nonimbibed one. The former is considerably
larger, and also lighter in color, than the latter.
Data analysisFor each species, a one-way (with collection date)
ANOVA followed by Tukeys multiple comparison test (SAS, 1988)
was conducted for all measurements except mass and moisture content
of pulp and endocarp. However, only length data are presented in this
paper, since the pattern for width was exactly the same as that for length
in both species. The square roots of all percentage data (i.e., moisture
content, germination percentage, and imbibition percentage) were arcsine-transformed prior to statistical analyses.

1219

TABLE 2. Comparison of the major flower/fruit developmental events

in Rhus aromatica and R. glabra in 1996.

R. glabra

%MC 5

RHUS

WAA (weeks after

anthesis)
Event

R. aromatica R. glabra

Anthesis
Endocarp physically separable from mesocarp
Cotyledons distinguishable
Fruit at maximum size
Cotyledons at maximum size
Embryo of most seeds germinable
Fruit red
Fruit at physiological maturity
Endocarp of most fruits impermeable to water

0
4
4
5
7
7
7
8
9

0
1
3
4
6
6
6
6
7

a Peak anthesis in 1996 was 18 April for R. aromatica and 27 June

for R. glabra.

RESULTS
General morphology of mature female flower, fruit,
and seedPlants of both R. aromatica and R. glabra at
the study site are strictly functionally dioecious, and
flowers of the two sexes in both species are dimorphic in
size and in structure. However, only information on pistillate flowers is presented in this paper. Individual flowers in both species are quite small at anthesis (18 April
for R. aromatica and 27 June for R. glabra in 1996)
(Table 1). The inconspicuous flowers are, however, clustered terminally on branches in strikingly conspicuous
inflorescences, which were 8.27 6 0.03 (mean 6 SE, N
5 50) cm and 15.7 6 0.05 cm long in R. aromatica and
R. glabra, respectively. The flowers (yellowish in R. aromatica and greenish in R. glabra) are typically pentamerous with an orange intrastaminal disc less than 2 mm
in diameter. Six- or even seven-numbered corollas and
calices were encountered infrequently in R. glabra. The
small unilocular ovary in both species encloses an anatropous ovule with a long curved funiculus attached basally to the placenta.
After ;2.0 and ;1.5 mo, the initially inconspicuous
ovary of R. aromatica and of R. glabra had developed
into a mature, attractive drupe; drupes of R. aromatica
are larger in size and in mass than those of R. glabra.
Accordingly, the endocarp, seed coat, and cotyledons in
R. aromatica are larger than those in R. glabra (Table 1).
The pale creamy seed coat in both species is characterized by a dark saddle-like patch, which originates from
the hypostase at the chalazal end of the ovule. The
creamy-colored cotyledons of both R. aromatica and R.
glabra are considerably flattened and bent.
General timetable of fruit and seed development
The time course of major developmental events for 1996
is shown in Table 2. In R. aromatica, the endocarp became physically separable from the rest of the fruit by 4
wk after anthesis (WAA hereafter), when the cotyledons
were just beginning to appear (i.e., embryo at heartshaped stage). By 5 WAA, the fruit reached its maximum
size, and by 7 WAA the embryo had grown to its full
length and width. This also was the time when most of
the embryos attained the ability to germinate and the fruit
turned ripe-red. After another week (8 WAA), physiological maturity was reached, which was 1 wk before the

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Fig. 3. Time course of growth in length of fruit (v), endocarp (),

seed coat (m), and cotyledons (,) in Rhus aromatica (a) and in R.
glabra (b) in 1996.

endocarp in the majority of fruits became impermeable

to water. This developmental sequence was very similar
in R. glabra, except for two minor differences. First, it
took only 1 wk for the endocarp of R. glabra to become
macrostructurally differentiated, as opposed to 4 wk in
R. aromatica. Second, all other major developmental
events occurred 1 wk sooner in R. glabra than the corresponding ones in R. aromatica, except physiological
maturity, which was reached at the same time that fruits
turned dark-red (ripe).
Pattern of growth in sizeGrowth curvesBoth R.
aromatica (Fig. 3a) and R. glabra (Fig. 3b) showed a
single-sigmoidal curve for growth in length for whole
fruit and for each fruit component. For R. aromatica, 5,
5, 6, and 7 wk of rapid growth resulted in fully expanded
whole fruit, endocarp, seed coat, and embryo, respectively. At the time the embryo reached its maximum size,
the fruit turned ripe-red, and the embryo attained the ability to germinate. Thereafter, sizes of whole fruit and fruit
components remained about the same until 9 WAA, when
the endocarp became impermeable to water; at this point,
all fruit and seed components began to shrink considerably. Exactly the same pattern of growth was observed
in R. glabra, except for the whole fruit and all of its
components, which reached maximum size 1 wk sooner.
In other words, the whole fruit, endocarp, seed coat, and
embryo in R. glabra grew rapidly until they attained their
full lengths and widths by 4, 5, and 6 WAA, respectively.
Then, there was no noticeable change in size until 7
WAA, when impermeability developed in the endocarp.
Again, the time when cotyledons reached their maximum
size was synchronized with the time of color change in
the fruit from green to red and with the embryo becoming
able to germinate.
The sigmoidal growth curve was repeated for all mea-

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Fig. 4. Comparison of growth in length of fruit (a), endocarp (b),

seed coat (c), and cotyledons (d) in Rhus aromatica in 1996 (V) and
in 1997 (v).

surements in 1997 for both R. aromatica (Fig. 4) and R.

glabra (Fig. 5).
Sequence of length growth among different componentsThe order of attainment of maximum size in both
R. aromatica (Fig. 3a) and R. glabra (Fig. 3b) in 1996
was fruit, seed coat, and cotyledons, each separated by 1
wk. The fruit had grown to full size by 5 and 4 WAA in
R. aromatica and R. glabra, respectively. One week later,
the seed coat reached its maximum length and width, and
in still another week the cotyledons grew to their mature
size.
Patterns of growth in length of fruit components in R.

Fig. 5. Comparison of growth in length of fruit (a), endocarp (b),

seed coat (c), and cotyledons (d) in Rhus glabra in 1996 (V) and in
1997 (v).

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RHUS

1221

accumulation in whole fruit (Fig. 6a, c) and in seed plus

endocarp (Fig. 6b, d). Growth rate was much higher in
R. aromatica (Fig. 6a, b) than in R. glabra (Fig. 6c, d),
as indicated by the much steeper slopes for R. aromatica.
Mass increase of whole fruit in R. aromatica was faster,
and maximum dry masses of both whole fruit and seed
plus endocarp were greater in 1996 than in 1997. In contrast, the pattern of mass increase of R. glabra in 1996
and 1997 was identical.

Fig. 6. Time course of dry mass accumulation (a) in fruit and (b)
in seed plus endocarp of Rhus aromatica and (c) in fruit and (d) in seed
plus endocarp of R. glabra in 1996 (V) and in 1997 (v).

aromatica in 1996 and in 1997 are shown in Fig. 4. The

whole fruit, endocarp, and seed coat reached mature size
at the same time in both years. However, the embryo
reached full size by 7 WAA in 1996 and by 9 WAA in
1997.
The fruit development pattern in R. glabra was exactly
the same in 1996 and 1997 (Fig. 5). As stated above, the
pericarp reached maximum size at 4 WAA; 1 and 2 wk
later, the seed coat and embryo, respectively, also had
grown to full size. Anthesis and thus all subsequent developmental events were 1 wk later in 1997 than in 1996.
Pattern of growth in dry massGrowth curvesAs
in length growth, both R. aromatica and R. glabra
showed a single sigmoidal growth curve for dry mass

Physiological maturityAccumulation of dry mass in

whole fruit, seed plus endocarp, pulp, endocarp, and seed
(ovule) in 1997 is shown in Table 3. For both species,
physiological maturity was reached at the same time (i.e.,
9 WAA for R. aromatica and 6 WAA for R. glabra) for
all components except the endocarp, which attained its
maximum dry mass 1 wk later (10 WAA for R. aromatica and 7 WAA for R. glabra) and became impermeable
to water. In other words, the endocarp was the first fruit
component to reach full size (Figs. 4, 5) and the last one
to reach physiological maturity, which coincided with the
development of its impermeability to water.
Mass allocation to different fruit componentsThe
two species also are quite similar in terms of mass allocation to fruit components. Throughout the course of fruit
development, most of the dry mass was allocated to the
pulp and endocarp in both R. aromatica (Fig. 7a) and R.
glabra (Fig. 7b). At the time the pericarp reached its
maximum size (5 and 4 WAA in R. aromatica and R.
glabra, respectively), only ;67% of the total dry mass
had been allocated to the seed. However, these values
increased to ;22% in R. aromatica and to ;16% in R.
glabra at physiological maturity. By the time the endocarp became impermeable, ;37% of the mass had been
allocated to the endocarp in both R. aromatica and R.
glabra. Pulp was the major allocation site, consisting of
;50% of the total dry mass at maturity.

TABLE 3. Comparison of dry mass (mg) accumulation in fruit and fruit components of Rhus aromatica and R. glabra in 1997.
WAAa

Fruit

R. aromatica
3
4
5
6
7
8
9
10

3.06
4.84
12.33
19.49
27.45
34.58
40.85
38.12

6
6
6
6
6
6
6
6

0.12abb
0.13b
0.26c
0.36d
1.23e
0.62f
0.43h
1.18g

R. glabra
2
3
4
5
6
7

2.72
7.37
9.35
12.55
13.81
13.99

6
6
6
6
6
6

0.28b
0.19c
0.24d
0.33e
0.22f
0.27f

Seed plus endocarp

Exocarp plus mesocarp

Endocarp

Seed

4.20
11.27
13.84
17.87
20.79
20.66

6
6
6
6
6
6

0.14a
0.10b
0.68b
0.64bc
0.23c
1.22c

8.13
8.22
13.61
16.70
20.06
17.46

3.96
9.33
10.43
11.22
11.89
13.99

0.07
0.12
0.24
1.94
3.41
5.29
8.90
6.67

0.41
2.45
4.47
5.68
6.67
6.96

6
6
6
6
6
6

0.02a
0.11b
0.05c
0.08d
0.05e
0.16e

2.31
4.62
4.88
6.87
7.14
7.03

0.38
2.40
3.83
4.34
4.52
5.15

0.024
0.049
0.64
1.34
2.15
1.81

6
6
6
6
6
6
6
6

0.01ab
0.01a
0.02ab
0.09b
0.18bc
0.15c
0.05d
0.62c

6
6
6
6
6
6

0.00a
0.00a
0.09b
0.07c
0.04d
0.08d

WAA, weeks after anthesis (17 April for R. aromatica and 3 July for R. glabra).
Means within each column for a species followed by the same letter are not significantly different at the 5% level as determined by Tukeys
multiple comparison test.
b

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TABLE 4. Comparison of moisture content (%) in exocarp plus mesocarp, endocarp, and seed (ovule) of Rhus aromatica and R. glabra
in 1997.
WAAa

R. aromatica
0
3
4
5
6
7
8
9
10

Fig. 7. Dry mass allocation to exocarp plus mesocarp (V), endocarp

(m), and seed () of (a) Rhus aromatica and of (b) R. glabra in 1997.

Moisture contentComparison between R. aromatica

and R. glabra in 1997The endocarp had the lowest
moisture content among fruit components at all developmental stages and was similar in R. aromatica and R.
glabra (Table 4). Moisture content decreased from ;82
84% at the time it became physically separable from the
rest of the fruit to ;10% when it became impermeable
to water. However, before impermeability developed the
pulp of the R. aromatica fruit had a higher moisture content than that of R. glabra. At that time, the fleshy part
of the fruits of both species had a moisture content of
;25%.

R. glabra
0
1
2
3
4
5
6
7

Exocarp plus
mesocarp

87.19
89.04
83.68
80.47
70.46
25.92

70.35
62.70
58.54
54.81
45.07
24.35

Endocarp

Seed

84.16
58.74
53.54
41.37
35.84
13.59

87.8
91.21
92.26
90.49
87.95
78.88
69.28
55.43
16.42

6
6
6
6
6
6
6
6
6

2.14ab
1.34a
0.87a
0.67a
0.61a
0.44b
0.64c
0.43d
0.56e

82.45
60.07
41.04
40.26
33.14
8.86

71.30
73.25
81.01
84.69
77.89
60.53
39.72
9.15

6
6
6
6
6
6
6
6

3.45a
3.33a
3.21a
2.43a
1.62b
1.32c
5.11d
2.54e

a WAA, weeks after anthesis (17 April for R. aromatica and 3 July
for R. glabra).
b Means within each column for a species followed by the same letter
are not significantly different at the 5% level as determined by Tukeys
multiple comparison test.

as peach, apricot, plum, and cherry, that growth of stony

fruits is characterized by a sequence consisting of rapid
growth, depressed growth, and a final rapid swell (Connors, 1919; Lilleland, 1932; Bollard, 1970; Coombe,
1976). In fact, Toldam-Andersen and Hansen (1997)
claimed that this double-sigmoidal growth pattern is characteristic of fruit growth in general. However, contrary
to the shape of the growth curve of typical drupes of
these commercial crops, that of R. aromatica and of R.

Variation between 1996 and 1997At similar developmental stages, both fruit (Fig. 8a) and seed plus endocarp (Fig. 8b) of R. aromatica had a higher moisture
content in 1997 than in 1996. However, no differences
were observed between 1996 and 1997 in R. glabra (Fig.
8c, d).
Relationship between embryo germinability and endocarp impermeabilityMoisture content of the embryo at
the time it became germinable and of the endocarp when
it became impermeable was similar in R. aromatica (Fig.
9a) and R. glabra (Fig. 9b) in 1996. As the moisture
content of seed plus endocarp decreased from ;60% to
;40% in both species, the embryos changed from green
to creamy in color and became germinable. However, endocarp impermeability did not develop until moisture
content of seed plus endocarp dropped to below 20% in
both species. It took 2 wk for the transition from permeability to impermeability of the endocarp in R. aromatica and 1 wk in R. glabra.
DISCUSSION
Since early this century, it has been shown repeatedly
in some commercially cultivated drupaceous fruits, such

Fig. 8. Time course of moisture content (a) in fruit and (b) in seed
plus endocarp of Rhus aromatica and (c) in fruit and (d) in seed plus
endocarp of R. glabra in 1996 (V) and in 1997 (v).

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Fig. 9. Germinability of embryo (v) and impermeability of endocarp (m) in relation to moisture content of seed plus endocarp () in
Rhus aromatica (a) and in R. glabra (b).

glabra followed a single-sigmoidal pattern for increase

in both size and mass, which is similar to what has been
reported for some nondrupaceous fruits such as apple
(Denne, 1960), pear (Bain, 1961), castor bean (Greenwood and Bewley, 1982), and ash (Wagner, 1996). Similar deviations from the double-sigmoidal growth curve
also were observed in almond (Brooks, 1939), date (Haas
and Bliss, 1935), and avocado (Schroeder, 1953). Searching for an explanation for the single-sigmoidal pattern of
growth, Bollard (1970) pointed out that the almond has
a dry leathery mesocarp vs. the fleshy ones of typical
drupes; thus, the almond lacks a swelling stage. Although
the mesocarps of R. aromatica and R. glabra are reasonably fleshy (moisture content of 4589%) prior to maturation desiccation, they become dry (;25% moisture
content) after impermeability develops in the endocarp.
In both R. aromatica (Fig. 3a) and R. glabra (Fig. 3b),
the temporal sequence of attainment of maximum size
was fruit, seed coat, and embryo, which is similar to that
of Fraxinus excelsior (Wagner, 1996). This pattern of
seed development lagging behind that of fruit development also has been reported in Rhus lancea (von Teichman and Robbertse, 1986b) and in other genera (Copeland, 1961; von Teichman and Robbertse, 1986a; von
Teichman, 1987) of the Anacardiaceae. However, whereas the time lag between attainment of maximum size of
pericarp and of seed in R. aromatica and R. glabra is
only 12 wk, in other taxa of Anacardiaceae it is 520 wk
(Grundwag, 1976; von Teichman and Robbertse, 1986b;
von Teichman, 1991a; Shuraki and Sedgley, 1996).
Reproductive development of R. aromatica and R. glabra at the study site is separated by ;2 mo. For example,
the week after the endocarp of R. aromatica fruits became impermeable to water R. glabra was at peak anthesis (20 June27 June in 1996 and 26 June3 July in
1997). However, there are similarities in the timetable and

RHUS

1223

in the pattern of the morphology and physiology of fruit

and seed development in these two species.
The pericarp reached its maximum size (length) much
earlier than it reached its maximum mass in both R. aromatica and R. glabra (6 vs. 9 wk in R. aromatica and 4
vs. 7 wk in R. glabra), whereas the embryo reached its
maximal size and mass at the same time (i.e., 1 wk before
impermeability developed) in both species (9 wk in R.
aromatica and 6 wk in R. glabra). For both R. aromatica
and R. glabra, the endocarp was the last fruit component
to reach physiological maturity. These results are in contrast to those reported by Lilleland (1932), who showed
that the stone of peach attained its maximum mass before
either flesh or seed.
Allocation of fruit dry mass to the endocarp in both R.
aromatica and R. glabra varied from ;15% early in development to ;37% at maturity (Fig. 7), which is much
lower than that allocated to the mature endocarp in hackberry (Cowan et al., 1997), but higher than that allocated
to the mature endocarp in peach (Lilleland, 1932).
Compared to 1996, size growth of the embryo in R.
aromatica was delayed by 2 wk in 1997 (Fig. 4d), while
in R. glabra it was the same in 1996 and 1997 (Fig. 5).
Compared to R. glabra, there was a delay in increase in
dry mass and in attainment of final mass of fruit and of
seed plus endocarp in R. aromatica (Fig. 6). Further,
whereas the time course of development of fruit and of
seed plus endocarp in R. glabra was identical in 1996
and 1997, in R. aromatica there was a lag period of ;1
wk in 1997 compared to 1996. This difference in the time
course of growth in R. aromatica most likely is due to
the variation in temperature and precipitation during the
study period. Early summer 1997 was much cooler and
wetter at the study site in 1997 than in 1996 (Fig. 1). For
instance, mean monthly maximum temperature in both
May and June was ;58C cooler in 1997 than in 1996,
and precipitation in June 1997 was ;245 mm, which is
almost twice as much as that of June 1996 (125 mm).
Presumably, the warm-dry conditions in late springearly
summer 1996 were more favorable for fruit growth and
development than were the conditions in 1997. However,
the cool, wet weather of 1997 did not continue for the
rest of the summer, and thus did not affect R. glabra,
except by delaying anthesis for 1 wk (26 June in 1996
and 3 July in 1997). In fact, moisture content data for
fruit and for seed plus endocarp (Fig. 8) support this
speculation. At similar developmental stages prior to the
onset of endocarp impermeability, moisture content of
whole fruit and of seed plus endocarp of R. aromatica
was higher in 1997 than in 1996. On the contrary, no
such difference was observed between these two years in
R. glabra.
It took only 89 wk for the small flowers of R. aromatica and 6 wk for those of R. glabra to develop into
conspicuous mature red fruits. These developmental periods are considerably shorter than those reported for other members of the Anacardiaceae, including R. lancea, a
Southern African species (von Teichman and Robbertse,
1986b; von Teichman, 1991a), Protorhus (von Teichman,
1991b), and Pistacia (Grundwag, 1976), which take 13,
15, and 20 wk, respectively, for fruit development. In R.
aromatica and R. glabra, the change in color of fruit from
green to red coincided with color change of the embryo

1224

AMERICAN JOURNAL

from green to creamy and its ability to germinate; soon

afterwards, maturation desiccation resulted in endocarp
impermeability to water.
In general, seed development and acquisition of the
ability to germinate are associated with an overall loss of
moisture (Adams and Rinne, 1980), and this was absolutely true for R. aromatica (Fig. 9a) and R. glabra (Fig.
9b). Germinability of the embryo was coupled with a
decrease in moisture content of the seed plus endocarp
unit. Most embryos of both species attained the ability to
germinate after the moisture content of the seed plus endocarp decreased to below 20%.
In both R. aromatica and R. glabra, development of
endocarp impermeability was synchronized with attainment of physiological maturity, which was 1 wk after the
dry mass of other components of the fruit had peaked.
Thus, it seems that deposition of some chemical(s) in the
endocarp may be coupled with desiccation, resulting in
an increase in endocarp mass and in its impermeability
to water. It would be interesting to investigate the effect
of artificially decoupling the effects of these two factors
on the development of endocarp impermeability, e.g., by
collecting fruits immediately before the endocarp reaches
physiological maturity and then artificially desiccating
the seeds.
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