Variation in the Phenology of Natural Populations of Montane ...

Variation in the Phenology of Natural Populations of Montane Shrubs in New Zealand
Author(s): Richard B. Primack
Source: Journal of Ecology, Vol. 68, No. 3 (Nov., 1980), pp. 849-862
Published by: British Ecological Society
Stable URL: http://www.jstor.org/stable/2259460
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Journal of Ecology (1980), 68, 849-862
VARIATION IN THE PHENOLOGY OF NATURAL
POPULATIONS OF MONTANE SHRUBS IN NEW ZEALAND
RICHARD B. PRIMACK*
Department of Botany, University of Canterbury, Chhristchurch 1, New Zealand
SUMMARY
(1) Variation in flowering time of individuals in one population of each of three
species of shrub was recorded over two growing seasons in montane scrub-grassland
in the South Island of New Zealand.
(2) There was considerable variation in flowering time within each popuLlation, but
the flowering rank-order of individuals in different years was positively correlated.
(3) Variation in flowering time was poorly correlated witlh the dLuration of
flowering and the number of flowers and fruits per plant, except that variation in
flowering time in Discaria toumatou (Rhamnaceae) was weakly positively correlated
with the percentage fruit set in 1976-77. If both earlier and later flowering plants
showed reduced fruit set this would suggest stabilizing selection, but there is no
indication of such a pattern. Weak and inconsistent directional phenotypic selection
for flowering time can be demonstrated for these two species however.
(4) In the warm, dry summer of 1977-78, Leptospermum scoparium (Myrtaceae)
and Dracophyllumn spp. (Epacridaceae) flowered on average 9 days and 5 days
earlier respectively and for 17 and 8 days shorter duration than in the cool, damp
summer of 1976-77. Further, L. scoparium plants had a lower production of flowers
and fruits in the second season in comparison with the first season. Plants of
Discaria toumatou also flowered earlier in 1977-78, but the duration of flowering
and flower and fruit production was greater in 1977-78 than in the 1976-77 season.
(5) Patterns of variation in flowering time are also apparent among adjacent
populations depending on altitude and on the major geographical units of the
range of species. Variation in flowering time both at the individual and the population
level may be an important adaptation by which selection and physiological
mechanisms increase reproductive success.
INTRODUCTION
Most species flower at a characteristic time during the year at a particular locality, but
many species show gradual changes in flowering time over geographical and environmental
gradients (Jackson 1966; Harris 1970; Hodgkin & Quinn 1978). Such differences
might be environmentally or genetically controlled (or both). The existence of genetic
variation for flowering time within populations is known for a large number of plant
species (for examples, see McMillan & Pagel 1958; McIntyre & Best 1978). Despite a
sustained interest in flowering phenology (Robertson 1924; Heinrich 1976; Schemske
1977; Schemske et al. 1978; Poole & Rathcke 1979), little is known about variation in
flowering time within natural populations, in particular with relation to the reproductive
success of those plants. The work reported here was an investigation of variation in
* Present address: Biology Department, Boston University, Boston, Massachusetts 02215, U.S.A.
0022-0477/80/1100-0849 $02.00?01980 Blackwell Scientific Publications
849

850 Flowering-time variation
flowering time and reproductive capacity of three New Zealand montane shrub species
over a 2-yr period.
THE STUDY AREA
The shrubs grew in the scrub-grassland on Cass Hill, above the University of Canterbury
Field Station, Cass, Upper Waimakariri River Basin, South Island, New Zealand
(43?02'S latitude; 171?45'E longitude) at an altitude of 600 m (Plate 1). The ecology of
PLATE 1. Study site with plants of Discaria toumnatou (70 cm in height) in the foreground and
Leptospermum scoparium (c. 100 cm in height) in the background.

RICHARD B. PRIMACK 851
this area is described by Hayward (1967), Knox (1969), Burrows (1977) and Primack
(1978a). Forest of mountain beech, *Nothofagus solandri var. cliffortioides, originally
covered this area but was burned off in the 19th century by European settlers. The
vegetation is now dominated by native tussock grasses, herbs, and shrubs which were
previously restricted to stream and river edges, rock outcrops and above the timberline.
The area is used primarily for sheep grazing. The growing season lasts approximately
from October to March, with yearly averages of 9 ?C for temperature, 130 cm rainfall,
and 4.9 m s-1 wind speed (Burrows 1977). The soils are strongly leached high-country
yellow-brown earths (Cutler 1977). The spring is wet and cool, with the summer drier
and hotter, though the weather is highly variable among seasons and even from day to day.
The weather was cooler and wetter than usual in the spring and summer of 1976-77, while
it was warmer and drier than usual in the spring and summer of 1977-78.
A progression of flowering occurs throughout the growing season among the shrubs
and herbs of this study area. There are far more shrub flowers open at any time than there
are herb flowers, and the shrubs are therefore, probably, a far more important source of
nectar and pollen for most insects than are herbs. The flowers of all of the common species
of shrubs are visited by a wide range of insects, except for the Dracophyllum spp. which
are pollinated primarily by moths (Primack 1978b & unpublished). The shrub species
flower in a regular progression throughout the spring and summer, beginning with
Corokia cotoneaster then Gaultheria crassa and Discaria toumatou in late November;
Dracophyllum spp., Pimelea traversii, Olearia virgata and Leptospermum scoparium in
December; Hebe salicifolia and H. brachysiphon in January; followed by Cassiniafulvida
and Olearia avicenniaefolia in February. At times the progression of flowering is quite
striking, with one shrub species coming into flower as another species finishes.
MATERIALS AND METHODS
Two species and one hybrid complex were examined in this study.
(i) Discaria toumatou Raoul (Rhamnaceae) is a widespread spiny shrub endemic
in New Zealand. The small fragrant flowers have four or five white reflexed sepals and
no petals, and are produced either singly or in fascicles. Individual flowers last, on
average, for 3 days (range 1-5 days). The plants are self-infertile (Primack 1979). Natural
fruit set is only 700 and is partially limited by insect pollinator activity (Primack 1979;
Lloyd, Webb & Primack 1980). The fruit is a dry, three-lobed capsule containing an
average of 1.8 seeds (S.D. = 0.2).
(ii) Leptospermum scoparium J. R. et G. Forst. (Myrtaceae) occurs widely throughout
New Zealand in many habitats. The flowers are terminal or axillary with five white petals
and twenty-six stamens per flower. Individual flowers last from 1 to 3 weeks. The species
is andromonoecious. The perfect flowers tend to open in the first flush of flowering,
followed by the staminate flowers (Primack & Lloyd 1980). Individual plants within the
Cass Hill population showed considerable variation in the percentage of perfect flowers
(0-60%), with much of this variation environmentally induced (Lloyd, Webb & Primack
1980; Primack & Lloyd 1980). Hand-pollination of flowers does not increase fruit set, indicating
that pollinator activity is not limiting fruit set. The fruit is a woody capsule with
slits in the top which allow the numerous, tiny seeds to shake out.
(iii) The hybrid complex investigated was between Dracophyllum acerosum and D.
uniflorum Hook. f. (Epacridaceae). Hybrids are common in this genus (Allan 1961).
* Nomenclature follows that of Allan (1961).

852 Flowering-time variation
These two species are similar, both being much-branched shrubs with linear leaves. The
solitary, white, tubular flowers are fragrant in the evening. Individual flowers last on
average for 5 days (range 1-9 days). The fruit is a capsule. D. acerosum has longer leaves
(7-20 cm) than D. uniflorum (2-4 cm).
These shrub species can occur both as scattered individuals and in dense thickets.
Individual plants are variable in growth form, occurring as small, prostrate plants, as
shrubs, and as small trees. The plants in this study were mainly between 30 and 150 cm
in height. It is not possible to assess the age of these plants accurately because many
individuals sprout from a single base, but many of the shrubs in this area may be several
decades old (Primack 1978a).
Flowers of Discaria* and Leptospermum are visited during the day by a wide range of
nectar and pollen-collecting insects, particularly tachinid flies and halictid and colletid
bees (Primack 1978b). At night the flowers are visited by many species of noctuid and
pyralid moths. The flowers of Dracophyllum are pollinated at night by moths, though
occasional bees and flies visit the flowers to collect pollen during the day. These pollinator
assemblages vary considerably with time of day and weather (Primack 1978b).
Forty Discaria plants and forty Leptospermum plants on a hillside grassland area
approximately 10 x 10 m were labelled. The study population of thirty-five Dracophyllum
plants was 100 m away. During the 1976-77 and 1977-78 flowering seasons, the
total number of flowers open on each plant was counted at frequent intervals (every 2 to
4 days as a rule). A flower was judged to be open if the perianth and stigma were fresh in
appearance and undamaged. All counts of flowers on a given day were made by one
person.
Additional information was collected where possible for characters which might be
related to individual reproductive success. For Discaria and Leptospermum, the total
number of flowers and fruits produced by each plant was counted in both seasons. For the
Discaria plants in the 1977-78 season, the number of seeds per fruit was determined for a
sample of ten to twenty fruits per plant. The seeds of Dracophyllum and Leptospermum
were too small and too numerous to count individually.
The flower census allows a determination to be made of the date on which the plant
had the maximum number of flowers open. For Dracophyllum, the spread of dates of
maximum flowering is so large that an uncertainty of a day or two does not obscure
differences between individual plants. For Discaria and Leptospermum the spread is
smaller, so a correction factor was added to the date of maximum recorded flowering to
give a corrected date, the date of peak flowering. The correction factor was calculated as
the number of flowers open on the census date immediately after the maximum flowering
date minus the number of flowers open on the census date immediately before the maximum
flowering date, divided by whichever is larger. The correction factor has the effect
of shifting the maximum flowering date either forward or backward one day at most,
depending on the number of flowers open on a plant on the dates immediately before and
immediately after the maximum flowering date. Consequently, the peak flowering date
is a more accurate estimate of the date on which the plant had the most flowers open.
Other correction factors that take into account the number of days between samples
could have been used.
* The three taxa observed are referred to hereafter by generic name only.

RICHARD B. PRIMACK 853
RESULTS
Variation in flowering time
Within each of the populations there is considerable variation among individuals in
flowering time in both seasons (Figs 1-3). There is a regular progression of plants coming
into flower. Early-flowering plants finish flowering before many of the later plants come
40 1976 .*
30 -
20 -
10 _ *
24 29 1 3 5 7 9 13 17 19 21 24 26
O November December
40
1977
*
30 -
20 - _
6
I10
O E @6
24 29 2 5 8 1 1 14 17 2 1 26
November
December
FIG. 1. Flowering dates of forty Discaria toumatou plants in 2 yr in New Zealand arranged in order of
peak flowering date. Dates on the time axis are those on which the population was examined. Each
horizontal line represents the total duration of flowering for a plant. The heavy dot is the day of peak
flowering. The arrow-head brackets enclose the period during which the number of flowers open on
the plant was at least 50%0 of the maximum.

854 Flowering-time variation
40 - 1976-77 _ _ ____
< >
30-- ,
20~~~~~~~~~~~~~~~~~~~~~~
20 - -
10 9 - ,
24 26 28 30 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 2 4 7 11
0
December Janur ry February
40 - 1 977-7B
L
30~ - ~ ~ ~
20~~~~~~ -
I-0
I~~~~~~~I
0 4
30 _ -
< t -
< 2 4
Decmbe
January
FIG. 2.Flowering dates of forty Leptospermum scoparium plants in 2 yr in New Zealand. See Fig. I
for an explanation of symbols.
into flower. This separation of flowering time is even more striking when the number of
open flowers per plant is also considered.
The period of time over which a plant flowers strongly (i.e. has open more than half
the maximum number of flowers) is usually about one-third of its total flowering time.
In most plants, the number of open flowers is small initially, increasing dramatically for
a few days, declining rapidly, and then tapering off over a few days. In a few plants, the
number of open flowers is skewed in time, with either strong flowering occurring at the
beginning of the flowering period (e.g. Discaria 9 in 1977, Fig. 1), or strong flowering continuing
until the plant abruptly ceases flowering (e.g. Leptospermum 1 in 1976-77, Fig. 2).
The flowering time of each plant overlaps with many other plants in the population,
but pollinator activity, and consequent gene exchange between a plant and other plants

RICHARD B. PRIMACK 855
35
-
1976-77
30 -
20~~~~~~~~~~~
-
10 _
11 16 18 21 24 26 28 30 1 3 5 7 9 I'l 1'3 15 I? 17 9 21 2J3 25 2'7 31 4
December
Jonuory
35 - 1977-78
20 __
11 16 18 21 24 26 28 30 4 7 9 1 13 15 17 1 21 2 25 37
1
70 5 21 2
-4.>~~~~~~~~~~~4
December
Jonuary
FIG. 3. Flowering dates of thirty-five plants of Dracophylluim spp. in 2 yr in New Zealand. See Fig. 1
for an explanation of symbols.
in a population, occurs primarily during the shorter period of abundant flowering. When
a plant flowers strongly, only a portion of the other plants in the population are similarly
flowering strongly and capable of exchanging genes. The degree of overlap in flowering
among individuals can be quantified by calculating for all possible pairs of n individuals,
c = a/b
where a is the number of census dates on which plants are flowering strongly, and b is
the number of census dates for whichever individual flowered strongly for the fewest
census dates. An index of overlap in flowering, Z, for the individuals in a population
would be
where the number of comparisons will be
N = n(n - 1)/2.
The index of overlap would be 1.0 with complete overlap and 0.0 with no overlap.
The indices of flowering overlap for the two successive seasons are 0.68 and 0.74 for
Leptospermum, 0.42 and 0.74 for Discaria, and 0*34 and 0.41 for Dracophyllum. Each

856 Flowering-time variation
_
c
27 ;,, z t mP N
*_
N+1 +1 +111
S
e Li e :!x' ^ O?~~~~0
_ :C 3 *
&O "
(I =+ + 1
-; o
4SNo?N+ 1+
c53n qji n 0
C) o^ Z: +l +l +l +l +l
*. 0 a,,,

RICHARD B. PRIMACK 857
population showed more overlap in the second year, but there are consistent differences
between the three species too. The low index of overlap in Dracophyllum may indicate a
reduced chance of gene flow within the population.
The number of plants flowering strongly is initially small, increases through the season,
and then again declines at the end of the flowering season. In particular, Discaria plants
continue to have a few flowers open long after the period of strong flowering has passed.
For the Leptospermurn population in the 1976-77 season, on January 5, 11, 17, 23 and 29,
there were 6, 16, 32, 29, and finally just 8 plants flowering strongly.
Such temporal separation of individual flowering times is a common pattern in
populations of all three taxa in both seasons, but the pattern is not repeated exactly in a
population in successive years due to differences in the duration of flowering both for
individual plants and for the population as a whole (Table 1). Plants flowered in the
second season earlier and their flowering duration was either longer or shorter than in the
first season in all three species (Table 1; Figs 1-3). These differences between seasons are
all highly significant (P < 0 01) using t tests.
Correlation of flowering with other variables
Discaria toumatou
In the 1976-77 season, but not in the 1977-78 season, peak flowering date showed a
positive significant (P < 0.05) correlation (Table 2) with the number of fruits per plant
and the percentage fruit set; later flowering plants had more fruits and a higher percentage
of fruit set than earlier flowering plants. Peak flowering date was poorly correlated with
the duration of flowering, the number of flowers per plant, and the number of seeds per
capsule.
Significant positive correlations among plants between seasons were apparent for the
peak flowering date (r = 0.63; P < 0.05; Fig. 4) and the duration of flowering (r =
0.76; P < 0.001).
Leptospermum scoparium
The date of peak flowering showed a significant (P < 0.05) correlation with the
percentage fruit set in 1977-78; earlier flowering plants had a higher fruit set than later
flowering plants (Table 2). The date of peak flowering was uncorrelated with any other
plant character.
Significant positive correlations among plants between seasons were evident for peak
flowering date (r = 0*57; P < 0.01; Fig. 4) and the duration of flowering (r = 035;
P < 0.05).
TABLE 2. Correlation coefficients (r) of peak flowering date of shrubs in New
Zealand with other plant characters; sample sizes in Table 1; values for numbers
of flowers and fruits produced per plant and the percentage of fruit set
were logarithmically transformed to correct for log-normal distributions (see
standard deviation in Table I)
Discaria toumatou Leptospermum scoparium Dracophyllum spp.
Peak flowering date with: 1976 1977 1976-77 1977-78 1976-77 1977-78
Duration of flowering 0 088 0 112 - 0.063 -0 115 0.272 -0.111
Number of flowers per plant 0 088 -0 037 0.234 0 269 -0 201 -0.175
Number of fruits per plant 0.383* -0 088 -0 045 -0 192
Number of seeds per capsule -0 109
Fruit set (%s) 0 420** -0-149 -0-189 -0.399*

858 Flowering-time variation
1 3 ( a
11_
9-
E
7-
C 5
3 - _ _ _ _ _ _ _-
1 3 5 7 9 1 1 13 15 17 1 9
Rank in December 1976
16 - (b)
15 -
13 -_
30
11 _
*
30 * 4 ) )
0 30 9 9
r-
5__
7 9 11 13 15 17 19 21 23 25 27
Rang in January 1977
1o a(c (
o~~~~~~Rn n eene 7 oJnay17
OD
30
-
2 0 30 9 19
Rank in December 1976 to January 1977
FIG. 4. Relationship between peak flowering date in 1976-77 and that in 1977-78. (a) Discaria
toumatou, (b) Leptospermum scoparium, (c) Dracophyllum spp.

RICHARD B. PRIMACK 859
35
30
0
20-
0
c
0
0
a-
J J A S 0 N D J F M A M
Month of flowering
FIG. 5. Seasonal distribution of flowering in Leptosperrnlrn scoparilum on the North (C:) and South
Island (U) of New Zealand, based on the number of herbarium specimens with open flowers collected
in each month. Distribution based on eighty-nine herbarium specimens from the South Island and 107
from the North Island. Only one specimen per collector was included for any particular year. The
assumptions and biases of this sampling method are considered in detail elsewhere (Primack 1976,
1978c).
Dracophyllum spp.
Peak flowering date was uncorrelated with the duration of flowering or the number of
flowers per plant in either season (Table 2).
Peak flowering date showed a striking positive correlation (r = 0 94; P < 0.01) among
plants between the two seasons (Fig. 4). The sequence in which the plants flower is almost
exactly repeated in successive years. There was a significant (P < 0.01) positive correlation
between seasons in the duration of flowering (r = 0.74).
Var-iation in flowering time bet ueen sites
Flowering occurred over 4-8 weeks in populations of these species at the study site.
Each one of these species has a wider flowering time when the entire geographical range
of the species is considered. For example, on Cass Hill, there is an altitudiinal progression
of flowering, with Leptospermum plants at the base of the hill (600 m) flowering about 10
days before the plants at the study site (700 m) and about 3 weeks before the plants neai
the top of the hill (850 m). Leptospernium also shows significant differences (P < 0.01;
XI = 50; n = 1) in flowering time between the North and South Islands of New Zealand
on the basis of herbarium specimens (Fig. 5). In the North Island of New Zealand,
Leptospermum plants flower abundantly over a prolonged 6-month period with a peak of
flowering in November and December. In the South Island, plants have a more pronounced
4-month period of flowering, with a peak later in December and in January.
DISCUSSION
The flowering period of a plant species may be restricted because plants which flower
earlier or later than the optimal time have a reduced reproductive capacity. In a coevolved
community of plants and animals, it might be that this stabilizing selection
occurred in the past so that relatively little genetic variation for flowering time remains in

860 Flowering-time variation
the population. In fact, in the populations under study and in other plant populations
there is considerable individual variation in flowering time. Numerous species have
genetic variation for flowering time both within and among populations (for example,
Harris 1970; Primack 1976), and there seems no reason why this should not be true in
these shrub populations too. On present evidence it is not possible to separate the genetic
and environmental components of the variation in flowering time. However, the highly
significant positive correlations for individual plants in flowering rank-order between
seasons indicate that this variation is either under genetic control or caused by relatively
permanent environmental effects, such as microsite differences or the nutrient status of
the plant (Jackson 1966).
Three hypotheses can be advanced to explain the genetic variation for flowering time
within populations of numerous species.
(i) Yearly variation in weather results in shifting selection pressures for flowering time,
with no genotype ideally suited to all weather patterns.
(ii) There may be selection for variation in flowering time since earlier-and laterflowering
plants may experience greater pollen dispersal due to lower density of
flowering plants (Schemske 1977). The seeds resulting from this increased gene
dispersal may have a greater fitness because of heterosis than seeds resulting from
lower gene dispersal during the average flowering time for the population.
(iii) Yearly variations in insect predators and vertebrate herbivores of the flowers and
fruits and dispersal agents of the seeds may result in varying selection pressures on
flowering time, since time of flowering is probably correlated with the time of fruit
maturation.
Stabilizing selection in natural populations for optimal timing of flowering is analogous
to artificial selection for flowering time to achieve maximum yield in many temperate
fruit trees. A compromise between selection for earlier-fruiting varieties to take advantage
of high prices early in the season, and later-flowering varieties to avoid frost
damage to the flowers, results in trees with flowering times adjusted for maximum profitability
(Janick & Moore 1975).
Models of populations often assume panmictic gene exchange. Numerous studies have
shown, however, that gene dispersal distances are leptokurtic in distribution, with the
possibility of gene exchange being much greater with close neighbours (Levin & Kerster
1974). This study and other phenological studies (McMillan & Pagel 1958) suggests the
possibility that variation in flowering time might result in positive assortative mating.
In all populations, there will be a tendency for early- and late-flowering individuals to
exchange genes primarily among themselves. The indices of overlap in flowering time
show that an individual may be unable to exchange genes with more than half its neighbours.
This pattern of assortative mating based on flowering time is repeated in successive
years due to the strong positive correlation in flowering rank-order among individual
plants between years (Fig. 4). Variation in flowering time among neighbouring populations,
as seen in Leptospermum, similarly restricts gene exchange between populations,
potentially increasing population differentiation.
Two extreme patterns of flowering may be imagined: species which flower massively
for a brief period and species in which a constant small production of flowers occurs over
a long period (Janzen 1967; Gentry 1974). Mass flowering has the presumed advantage
of attracting many pollinators, while sequential flowering may reduce the level of
geitonogamy (fertilization between neighbouring flowers on the same plant) and force
the pollinators to fly between plants. This research shows that there is considerable

RICHARD B. PRIMACK 861
variation within these shrub populations in the duration of flowering and the extent to
which the flowers on a plant open sequentially or simultaneously. If this variation is to
some extent genetically based, natural selection could shift these populations along the
continuum between the two extreme strategies. Intermediate strategies might be less
successful than either extreme, however.
All three study populations showed a shift towards earlier flowering in the second season.
Although the weather patterns of the two seasons were different, flowering occurred on
average only 4, 5, and 9 days earlier in the three populations. While the individual plants
in these species have some flexibility in flowering time, depending on the immediate
climate (as shown by shifts in flowering time for an entire population as well as the
variation in time shifts for individual plants), there are also factors which confine this
flexibility (as shown by the small number of days of the flowering-time shift and the
positive correlation for flowering rank-order among plants between years). Either these
plants have only a limited phenotypic plasticity for this character or they are not
particularly sensitive to changes in weather.
Populations showed different seasonal responses in the duration of flowering. Individuals
of Dracophyllum and Leptospermum had shorter flowering duration in the second
season than in the first, while the individuals of Discaria showed greater flowering
duration in the second season. The contrast between Discaria and Leptospermum for
these two seasons holds for other characters as well: Leptospermum individuals had
lower numbers of flowers and fruits per plant and a lower fruit set in the second season,
while Discaria individuals showed increases in all three of these characters in the second
season.
In Leptospermum, four sorts of variation in flowering time can be seen: among individuals
within the study population; among adjacent populations on Cass Hill along an
altitudinal gradient; between major geographical units of the range of the species; and
among successive seasons at the same locality. This variation in flowering time may
represent an important means by which this species adapts ecologically and physiologically
to its environment.
ACKNOWLEDGMENTS
This work was supported by the Miss E. L. Hellaby Indigenous Grasslands Research
Trust and the National Science Foundation. I thank E. Godley and D. Lloyd for the
initial ideas from which this project developed; J. Antonovics, T. Meagher, N. Elstrand,
S. Zielinsky and N. Bird for useful suggestions; and S. Pollard for help with the field
work.
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862 Flowering-time variation
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(Received 2 August 1979)