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482
Reproductive ecology and allometry of red pine
(Pinus resinosa) at the northwestern limit of its
distribution range in Manitoba, Canada
Alanna Sutton, Richard J. Staniforth, and Jacques Tardif
Abstract: Red pine (Pinus resinosa Ait.) has been described as a poor seed producer at its distribution range limit;
however, few studies have verified this claim or have examined the factors influencing the reproduction of the species.
In 2000, data were collected from 60 trees growing in Manitoba at the extreme northwest limit of the natural distribution range for this species. Cones per tree were counted and samples weighed and measured. Likewise, seeds per cone
were counted, measured, weighed, and tested for germination. Correlation and regression analyses compared measured
characteristics among cones, among individual trees, and among portions of tree crowns (north, west, south, and east
portions). Cone abundance among individual trees was significantly and positively correlated with stem diameter and
with basal area increment from 1 to 4 years preceding cone maturation. Cone size and fresh mass and seed abundance,
mass, and germination were not significantly correlated with individual trees or crown portions; however, seed number
per cone and seed size were found to be significantly and positively correlated with cone size. Germination success in
red pine increased with seed mass to a certain threshold value, beyond which more than 80% of the seeds germinated
no matter what their mass. Our data for 2000 and field observations for 1999 and 2001 showed that red pine at its
northwest limit of distribution range produced numerous cones and viable seeds.
Key words: red pine, Pinus resinosa, distribution limit, seeds, germination, cones.
Résumé : On a longtemps considéré que le pin rouge (Pinus resinosa Ait.) produisait peu de graines à la limite de son
aire de répartition. Peu d’études ont toutefois confirmé cette généralisation ou examiné les facteurs influençant la reproduction de l’espèce. En 2000, nous avons échantillonné 60 arbres croissant au Manitoba à la limite nord-ouest de l’aire
de répartition de l’espèce. Les cônes ont été dénombrés et des échantillons mesurés et pesés. De plus, les graines ont
été comptées, mesurées, pesées et des tests de germination réalisés. À l’aide d’analyses de corrélation et de régression
nous avons comparé les caractèristiques des cônes, des arbres et des portions de courronne, divisées selon leur exposition nord, ouest, sud et est. Les analyses montrent que l’abondance des cônes par arbre est significativement et positivement corrélée au diamètre de la tige, à hauteur de poitrine, ainsi qu’à l’accroissement radial pendant les années
précédent la maturation des cônes. La taille et la masse des cônes ainsi que l’abondance, la masse et le taux de germination des graines ne sont pas significativement corrélés aux variables décrivant les arbres ou les portions de couronne.
Le nombre et la dimension des graines sont toutefois significativement et positivement corrélés à la taille des cônes. Le
taux de germination est significativement corrélé à la masse des graines, jusqu’à un seuil critique au-delà duquel plus
de 80% des graines ont germé, indépendament de leur masse. Nos données pour l’année 2000 et nos observations pour
les années 1999 et 2001 montrent qu’à la limite nord-ouest de sa répartition, le pin rouge produit de nombreux cônes
et graines viables.
Mots clés : pin rouge, Pinus resinosa, limite de répartition, graines, germination, cônes.
Sutton et al.
Introduction
The northern distribution limits of many tree species are
restricted by unfavourable climates that cause interruptions
Received 13 September 2001. Published on the NRC Research
Press Web site at http://canjbot.nrc.ca on 8 May 2002.
A. Sutton,1 R.J. Staniforth, and J. Tardif. Centre for Forest
Interdisciplinary Research (C-FIR) and Department of
Biology, University of Winnipeg, 515 Portage Avenue,
Winnipeg MB R3B 2E9, Canada.
1
Corresponding author (e-mail: [email protected]).
Can. J. Bot. 80: 482–493 (2002)
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493
in the reproductive cycle and ultimately depress fecundity
levels (Black and Bliss 1980; Pigott and Huntley 1981;
Houle and Filion 1993; Tremblay et al. 1996, 2002). Red
pine (Pinus resinosa Ait.) populations are disjunct at the
northern limit of the species distribution and were once described as declining and rare because of failure to maintain
themselves (Haddow 1948). Schooley et al. (1986) later
found that red pine is susceptible to ovulate cone damage
due to frosts during its early development. Bergeron and
Brisson (1990) have suggested that low seed production, especially as a result of large fires, may contribute to the restricted range of red pine. Severe climatic conditions at the
northern limit of the distribution range may exaggerate this
DOI: 10.1139/B02-031
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Sutton et al.
phenomenon (Bergeron and Gagnon 1987). Other species
such as basswood (Tilia americana L.) (Pigott and Huntley
1981) and jack pine (Pinus banksiana Lamb.) (Houle and
Filion 1993) are limited by extreme climatic conditions at
the northern limit of their distribution ranges. Furthermore,
both black spruce (Picea mariana (Mill.) BSP) (Black and
Bliss 1980) and red maple (Acer rubrum L.) (Tremblay et al.
1996) have shown delayed seed development or low germination success at the northern limits of their distribution
range.
In addition to climatic factors, nonclimatic factors such as
habitat availability, competition, disturbance, and unfavourable fire regimes may contribute to setting distribution limits
(Sakai and Weiser 1973; Bergeron and Gagnon 1987;
Bergeron and Brisson 1990; Flannigan 1993; Roberts and
Mallik 1994; Bergeron et al. 1997; Meilleur et al. 1997;
Flannigan and Bergeron 1998). Within the boreal forest region, climate, disturbance, and soil characteristics including
nutrient status are the primary factors that limit northward
expansion for many species (Flannigan and Woodward 1994,
Flannigan and Bergeron 1998). In red pine, a combination of
climatic factors, habitat availability, competition, disturbance
regime (i.e., fire regime), and random extinctions may explain the northern distribution range limit (Bergeron and
Gagnon 1987; Bergeron and Brisson 1990; Flannigan 1993;
Bergeron et al. 1997; Flannigan and Bergeron 1998).
Red pine has thick bark and self-pruning abilities that allow it to survive light to moderate surface fires (Bergeron
and Brisson 1990) even when the associated vegetation is
killed (Butson et al. 1987). Surface fires rarely spread to the
upper canopy or kill the trees. Instead, fires remove competing vegetation, contribute to mineral seed bed preparation,
and open the canopy, all of which are advantageous events
for shade-intolerant species such as red pine. Recruitment
patterns of red pine seedlings are largely determined by the
occurrence of fires and the resulting formation of suitable
seed beds (Engstrom and Mann 1991). The management of
competing vegetation by fire or other means may be an important tool in the success of red pine plantations (McRae et
al. 1994; Johnson et al. 1998).
Several genetic techniques (Simon et al. 1986; Mosseler et
al. 1991, 1992; Deverno and Mosseler 1997) have demonstrated that there is a lack of genetic variability in red pine,
even amongst disjunct populations near distribution range
limits for the species. This characteristic is rare amongst
other conifer species (Deverno and Mosseler 1997). Low genetic variability in red pine populations may make this species vulnerable to rapid environmental change, e.g., global
climate change (Mosseler et al. 1992).
The reproductive biology of red pine has been thoroughly
documented (Lyons 1956; Duff and Nolan 1958; Mirov
1967; Dickmann and Kozlowski 1969a, 1969b, 1969c). Optimum cone production occurs between 50 and 150 years,
but a few ovulate cones may be formed on trees as young as
5 years (Rudolf 1990). Good crops occur at intervals of 3–7
years and mast crops every 10–12 years (Horton and Bedell
1960; Rudolf 1990; Sims et al. 1990). As in many species of
Pinus, cone primordium differentiation occurs 2 years prior
to dispersal of mature seeds (Dickmann and Kozlowski
1969b; Barnes et al. 1998; Keeley and Zedler 1998). More
483
cones are produced on vigorous young branches on the
southern sides of trees (Rudolf 1990), and cones in the upper
third of the crown or on the ends of main branches produce
most of the viable seeds (Lyons 1956). Seeds from the middle section of cones show the highest percent viability; however, the proportion of aborted seeds can be as much as 20–
100% in this species (Rudolf 1965, 1990; Sims et al. 1990).
Cone and seed production is often influenced by insects and
rodents (Lyons 1956). The seeds are dispersed by wind from
late August to mid-September (Rudolf 1965, 1990), with
germination occurring during the following spring or summer. Not much is understood about factors affecting size of
cone crops because of the length of time from cone initiation
to dispersal (Keeley and Zedler 1998).
Fraser (1951), Cayford (1964), Rudolf (1965, 1990), Stiell
(1988), Bergeron and Brisson (1990), and Sims et al. (1990)
have described red pine as a poor cone producer, although
no definitions of “good” and “poor” cone production or
“good” and “poor” seed production have been given. Cone
production is lower in the northern populations than in those
from the south and is considered by Sims et al. (1990) to be
rare near the northern edge of its distribution range. There is
much variation among individuals (Stiell 1988). This view
was, however, recently challenged by Flannigan and
Bergeron (1998) who observed successful germination of
red pine seeds near its actual northern distribution limit in
Quebec.
An understanding of the processes that affect distribution
range limits is needed to allow the prediction of future species responses to climate change. Flannigan and Woodward
(1994) have predicted that the southern limit of red pine will
migrate northward faster than its northern limit and that
there will be a drastic shift in the overall range of this species. It is necessary to understand the processes that govern
seed production and germination success at the northern
limit of the present distribution range because they may determine the extent and rate of northward expansion. The
biogeographical success of a species is ultimately decided
by its success in colonizing parcels of the earth’s surface
(Lanner 1998).
In this study, we examined how some biotic factors influence seed and cone production in red pine populations at the
extreme northwest of the species’ distribution range. Except
for studies by Flannigan and Woodward (1994) and
Flannigan and Bergeron (1998), the reproduction ecology of
red pine at the limit of its distribution range has not been
thoroughly studied. The primary objective was to evaluate
differences among trees (age, radial growth, height, diameter) and crown portions (aspect, shape, size) in terms of cone
production and seed characteristics and germination. The
second objective was to determine whether cone characteristics (size, mass, seed number) have an effect on seed characteristics (size, mass, germination success).
Methods
Study area
The study area was located on Black Island (51°10′ N,
96°30′ W) approximately 300 km north of Winnipeg
(Fig. 1). Black Island is located at the north end of the
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484
Can. J. Bot. Vol. 80, 2002
Fig. 1. Map showing the location of the red pine (Pinus resinosa) stand on Black Island, Lake Winnipeg, Manitoba. The location of
the town of Arborg (closest meteorological station) is also indicated.
southern basin of Lake Winnipeg. It is among the largest islands in Lake Winnipeg with an area of approximately
123 km2. The island lies in the transition between the Canadian
Shield and the Great Interior Plains of North America. Geologically, the eastern tip of the island has exposures of hard
granitic bedrock of the Canadian Shield that is overlain by
Ordovician sandstone and limestone toward the centre and
east end of the island (Manitoba Natural Resources (MNR)
1988; Goulet 1992). The surface deposits on Black Island
are predominantly coarse-texture glacial tills and silica
sands, the latter having eroded from the underlying sandstone. The island is covered by coniferous and mixed forests, dominated by white spruce (Picea glauca (Moench)
Voss), black spruce, trembling aspen (Populus tremuloides
Michx.), and jack pine (MNR 1988). Black Island provides
habitats for provincially rare plant species that include red
pine (MNR 1988; Staniforth and Tardif 2000).
Black Island has special religious significance for the aboriginal people living in the vicinity of Lake Winnipeg
(MNR 1988). Traditional ceremonies took place at the
eastern end of the island, and today the native people gather
annually on Black Island for berry picking and other activities (Barker 1979; MNR 1988). Forestry operations on Black
Island had been carried out for a number of years prior to
the creation of Hecla Provincial Park in 1969. Major timber
harvesting started in the early 1900s and extensive areas of
Black Island were cut over and are now covered in new
growth (MNR 1988). It is uncertain how much of the red
pine stand was harvested in the early twentieth century or
burnt by fires; however, some existing trees are at least 150
years old.
The red pine population on Black Island is the most northerly and westerly occurrence of the species in North America (MNR 1988). Most of the stand is intermixed with jack
pine, black spruce, balsam fir (Abies balsamea (L.) Mill.),
and white birch (Betula papyrifera Marsh.), with common
juniper (Juniperus communis L.), lichens, mosses, and a thin
litter layer covering the forest floor. Many seedlings and sap© 2002 NRC Canada
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Sutton et al.
485
Table 1. Basic statistics for red pine (Pinus resinosa) at the extreme northwest of the species’ range on Black Island, Manitoba (n = 60).
Variable
Height (m)
Diameter (cm)
Establishment date
Basal area increment (cm2)
1996
1997
1998
1999
2000
1996–2000
Total number of cones
Minimum
8.31
16.20
1883
0.70
1.08
1.12
0.35
0.86
4.11
0
lings of red pine were observed in the sample area, indicating that recruitment is successful. Evidence of past fires
included fire scars and charred stumps.
The climate of the region has been classified as Humid
Continental. The closest meteorological station is located at
Arborg (50°56′ N, 97°05′ W) 70 km southwest of the study
site. It has a frost-free period of approximately 110 days.
The mean annual temperature and total annual precipitation
for the reference period 1961–1990 were 0.9°C and 491 mm,
respectively. The mean daily January temperature is –20.2°C,
and the mean daily July temperature is 18.4°C. The mean
proportion of precipitation falling as snow is 22.4% (Environment Canada 1993).
Sampling procedures
Random sampling and nearest neighbour methods were
used to select a sample of 60 individual trees along a 550-m
transect at the top of a sand ridge. The sample was restricted
to trees having diameters at breast height (dbh) in the range
of 16–24 cm to exclude individuals that may have been reproductively immature and those too tall to allow cone collection. The sample trees were growing on acidic, sandy
soil. The canopy in this portion of the stand was generally
open. The position of each sample tree was recorded using a
global positioning system.
Tree and crown measurements
Height, dbh, age, and the number of cones were determined for each sample tree. Cone numbers were estimated
using binoculars during the third week of August 2000. To
estimate age, a core was extracted from the east side of each
stem base and later analyzed in the laboratory using
dendrochronological techniques. Annual basal area increments for the years 1996–2000 were also measured at that
time using a Velmex measuring system. Annual radial increments were transformed into annual basal area increments to
take into account the variation in diameter among trees.
The crown of each sample tree was divided into north,
east, south, and west portions, each of which was treated as
a distinct sample unit. This gave a total of 240 crown portions (i.e., four portions for each of 60 trees). For each portion, crown size and shape were characterized by measuring
the heights and lengths of both the lowest and longest living
branches. An estimate was made of the area of each crown
Maximum
16.92
23.80
1974
Mean
11.10
20.14
1949
SD
1.51
2.33
27.95
59.17
53.94
56.48
58.86
39.88
245.52
256
22.41
20.64
26.87
26.17
19.60
115.70
43.00
12.79
11.43
14.44
14.03
9.75
59.03
47.77
portion from tree height and branch measurements. For each
crown portion, the nearest neighbour tree species, distance,
diameter, and height were measured. The nearest neighbour
was defined as the closest living or dead tree having a height
close to 75% of the sampled tree. These data were then used
to calculate a competition index (CI) for each crown portion.
For each of the 240 crown portions, the nearest neighbour
tree distance, diameter, and height were transformed into
percent distance (RDis), diameter (RDia), and height (RH)
relative to the sampled crown portion. The competition
index that we had formulated was as follows: CI = ((100 –
RDis) + RDia + RH)/300. We subtracted the relative distance from 100 to inverse the scale so that close trees contributed more to the competition index than distant ones.
Therefore, the crown portion with the neighbour tree having
the largest dbh and height and the smallest distance would
have the largest competition index value. To complement
this index, a densiometer was used to measure the opening
of the canopy at the mid-distance between each tree and its
nearest neighbour for each crown portion. The number of
mature, closed cones per crown portion was estimated with
the help of binoculars.
Cone collection and measurements
Cones that had turned purple were considered mature by
Krugman and Jenkinson (1974) and Young and Young
(1992). On Black Island, this had occurred by midSeptember 2000, and a collection was made on September
16, 2000. Where possible, at least five cones were collected
from each of two randomly chosen crown portions from
each sample tree. Some trees had fewer cones at collection
time than at the time of cone abundance estimation because
of removal by red squirrels (Tamiasciurus hudsonicus
(Erxleben)). Red squirrels may remove cone-bearing branch
tips during the fall (Roe 1948). The 503 cones collected
from the 60 trees were put into paper bags and brought back
to the laboratory.
In the laboratory, each cone was put into a bag, labelled,
and stored at room temperature. Fresh mass, diameter, and
length were recorded within a week of collection. The cones
were then left to dry with sufficient aeration to prevent
molding. Further drying at 55°C for 9 h encouraged the
opening of the cones without damaging the seeds (Krugman
and Jenkinson 1974; Young and Young 1992). We extracted
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0.61
0.92
0.61
0.59
0.42*†
0.61
0.78
–0.20*
0.66*
0.21*
0.20*
0.22*
0.19*
0.09*
0.17*
0.19*
–0.32*†
–0.24*
–0.19*
–0.25*
–0.23*
–0.26*†
0.2*
0.68
–0.06*
0.31*†
0.12*
0.30*
0.28*
–0.29*
–0.13*
–0.02*
0.47
–0.76
0.36*†
–0.10*
0.07*
–0.00*
0.02*
0.21*
0.12*
0.22*
0.63
0.63
0.67
0.68
0.68
0.70
—
—
1.00
ED
0.45
–0.61
0.65
0.11*
0.06*
0.10*
0.08*
0.2*
0.22*
0.23*
1.00
0.88
0.84
0.80
0.65
0.89
—
—
—
Ba96
0.51
–0.59
0.64
0.10*
0.05*
0.08*
0.08*
0.16*
0.21*
0.13*
—
1.00
0.96
0.93
0.80
0.97
—
—
—
Ba97
0.53
–0.60
0.58
0.13*
0.14*
0.15*
0.14*
0.11*
0.19*
0.13*
—
—
1.00
0.95
0.88
0.98
—
—
—
Ba98
0.54
–0.65
0.61
0.8*
0.11*
0.10*
0.10*
0.18*
0.23*
0.14*
—
—
—
1.00
0.91
0.97
—
—
—
Ba99
*Not significantly correlated; all others values were significant at p = of 0.05 after a Bonferroni correction.
†
Values significant at p = 0.05 with uncorrected probability but not with Bonferroni correction.
—
1.00
0.28*†
1.00
0.28*†
–0.47
Height (Hei)
Diameter (Dia)
Establishment date (ED)
Basal area increment (cm2)
1996 (Ba96)
1997 (Ba97)
1998 (Ba98)
1999 (Ba99)
2000 (Ba00)
Total basal area (cm2), 1996–
2000 (TBA)
Crown area (CA)
Competition index (CI)
Total number of cones (TNC)
Mean cone length (MCL)
Mean cone diameter (MCD)
Mean cone area (MCA)
Mean cone fresh mass (MFM)
Mean seed mass (MSM)
Mean seeds per cone (MSC)
Germination success
Dia
Hei
Variable
0.47
–0.64
0.44*†
0.06*
0.14*
0.11*
0.09*
0.17*
0.21*
0.03*
—
—
—
—
1.00
0.89
—
—
—
Ba00
0.53
–0.65
0.62
0.11*
0.11*
0.12*
0.11*
0.18*
0.23*
0.15*
—
—
—
—
—
1.00
—
—
—
TBA
1.00
–0.22
0.46
0.12*
0.16*
0.15*
0.13*
0.15*
0.20*
0.16*
—
—
—
—
—
—
—
—
—
CA
—
1.00
–0.42*†
0.14*
0.05*
0.09*
0.12*
–0.23*
–0.19*
–0.19*
—
—
—
—
—
—
—
—
—
CI
—
—
1.00
0.13*
0.13*
0.14*
0.05*
0.20*
0.23*
0.06*
—
—
—
—
—
—
—
—
—
TNC
—
—
—
1.00
0.63
0.90
0.79
0.04*
0.17*
0.00*
—
—
—
—
—
—
—
—
—
MCL
—
—
—
—
1.00
0.90
0.89
0.13*
0.40*†
0.25*
—
—
—
—
—
—
—
—
—
MCD
—
—
—
—
—
1.00
0.93
0.10*
0.31*†
0.15*
—
—
—
—
—
—
—
—
—
MCA
Table 2. Correlation coefficient matrix showing relationships between characteristics of red pine (Pinus resinosa) on Black Island, Manitoba (n = 60).
—
—
—
—
—
—
1.00
–0.01*
0.19*
0.21*
—
—
—
—
—
—
—
—
—
MFM
—
—
—
—
—
—
—
1.00
0.84
0.12*
—
—
—
—
—
—
—
—
—
MSM
—
—
—
—
—
—
—
—
1.00
0.07*
—
—
—
—
—
—
—
—
—
MSC
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487
Table 3. Basic statistics for crown portion variables for red pine (Pinus resinosa) on Black Island,
Manitoba (n = 240).
Variable
Minimum
Maximum
Mean
SD
Lowest living branch height (m)
Lowest living branch length (m)
Longest living branch height (m)
Longest living branch length (m)
Crown length (m)
Total crown area (m2)
Total number of cones
Nearest tree distance (m)
Nearest tree diameter (cm)
Nearest tree height (m)
Competition index (%)
Densiometer (%)
0.12
0.16
0.73
0.30
3.70
0.99
0
0.54
1.32
5.83
21.60
0
6.66
4.57
10.77
3.41
13.78
20.10
82
15.75
54.80
23.65
81.22
24
2.35
1.03
5.49
2.09
8.76
10.76
10.75
5.33
18.02
11.65
49.33
18.54
1.43
0.55
1.52
0.59
1.33
3.69
13.21
3.23
8.58
3.55
11.49
6.33
Fig. 2. Relationship between cone (a) diameter and length,
(b) diameter and fresh mass, and (c) length and fresh mass for
red pine (Pinus resinosa) on Black Island, Manitoba.
Fresh mass (g)
Fresh mass (g)
(a)
(b)
(c)
approximately 30 seeds per cone using forceps beginning at
the base of the cone. The seeds were dewinged by hand and
weighed. For each seed, the straight length, straight width,
and projected area were determined using program
WinSeedle v. 5.0a (Régent Instruments 2000). The total
number of seeds was recorded for each cone.
Germination success was assessed for unstratified seeds
(Krugman and Jenkinson 1974; Young and Young 1992).
The seeds were first surface sterilized in a 5% solution of
Javex for 2 min and then rinsed in distilled water three times
for 1 min each time. They were then aseptically placed into
Petri dishes containing 15% weight by volume of
nonnutrient Difco agar and the Petri dishes sealed. Each dish
contained the seeds from one cone. The seeds were placed to
germinate for 30 days in a greenhouse having mean minimum and maximum temperatures of 18 and 27°C, respectively, and a 16 h light : 8 h night cycle. Krugman and
Jenkinson (1974) and Young and Young (1992) reported that
seeds of red pine germinate equally well in the presence or
absence of light. The Petri dishes were randomly placed and
periodically rearranged to negate any microclimate differences within the greenhouse. The number of germinants was
counted at 5-day intervals.
Statistical analysis
Statistical analysis used SYSTAT (v. 9) for Windows
(SYSTAT 1999). Pairwise Pearson correlations with
Bonferonni probabilities were done on each of the three categories of data (individual trees, crown portions, cones). For
comparisons among trees, correlation analyses compared
trends in tree height and tree diameter, establishment date,
basal area increments (1996–1999, 2000), total basal area increment (1996–2000), crown area, competition indices, and
total number of cones. For comparisons among crown portions, correlation analyses compared trends in height and
length of lowest living branches, height and length of longest living branches, bole length, crown portion area, total
number of cones, distance, diameter, and height of the nearest tree, competition index, and densiometer reading. For
comparison among cones, correlation analyses compared
trends in cone length, diameter, area, mass, mean seed mass,
number of seeds per cone, total seed mass, seed length, diameter, area, and germination success at 30 days. In addition, multiple regressions using backward selection were
done for the total number of cones per tree for comparisons
among trees and among crown portions.
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0.31
–0.19*†
0.12*
–0.00*
–0.06*
0.09*
0.06*
0.01*
0.10*
–0.04*
0.05*
–0.04*
0.10*
0.13*
0.07*
0.17*
0.01*
–0.07*
–0.32
0.24
0.18*†
0.19*
0.14*
–0.00*
0.19*
0.15*
0.17*
0.11*
0.04*
–0.22*†
0.16*†
0.08
0.09
0.01
0.13*
0.12*
0.10*
0.13*
–0.19*†
–0.27
–0.17*†
–0.03*
0.15*†
0.18*†
0.37
1.00
—
—
—
—
—
CPA
0.24
0.59
1.00
—
—
—
—
BL
–0.10*
0.31
0.31
0.89
0.27
1.00
—
—
—
Lgl
0.10*
–0.11*
–0.04*
0.12*
–0.07*
0.02*
1.00
—
—
Lgh
*Not significantly correlated; all others values were significant at p = 0.05 after a Bonferroni correction.
†
Values significant at p = 0.05 with uncorrected probability but not with Bonferroni correction.
0.09*
0.14*
0.04*
–0.23*†
0.08*
Mean cone fresh mass (MFM)
0.13*
–0.29*†
0.12*
Mean cone area (MCA)
0.12*
0.10*
–0.04*
0.02*
Mean cone diameter (MCD)
Germination success
0.19*
Mean cone length (MCL)
–0.07*
Mean seeds per cone (MSC)
0.31
Densiometer (D)
–0.07*
–0.18*
0.48
Competition index (CI)
–0.03*
–0.10*
0.03*
0.05*
0.30
–0.07*
0.36
–0.14*†
1.00
—
Lwl
Mean seed mass (MSM)
0.44
†
Nearest tree height (Nth)
Nearest tree distance (Nds)
0.23*
–0.31
Total number of cone (TNC)
Nearest tree diameter (Nda)
–0.40
–0.29
Crown portion area (CPA)
–0.29
–0.41
0.45
Longest living branch height (Lgh)
Bole length (BL)
0.11*
Lowest living branch length (Lwl)
Longest living branch length (Lgl)
1.00
Lwh
Lowest living branch height (Lwh)
Variable
–0.03
0.02
–0.10
0.07*
0.10*
0.11*
0.08*
–0.21*†
–0.32
–0.21*†
0.08*
0.33
1.00
—
—
—
—
—
—
TNC
–0.06*
0.11*
–0.13*
0.06*
0.11*
0.09*
0.11*
–0.46
–0.58
–0.01*
0.02*
1.00
—
—
—
—
—
—
—
Nds
0.01*
0.06*
–0.14*
–0.01*
–0.03*
–0.00*
–0.03*
–0.12*
0.74
0.7
1.00
—
—
—
—
—
—
—
—
Nda
–0.22*†
0.01*
–0.20*
0.08*
0.08*
0.04*
0.11*
–0.16
0.75
1.00
—
—
—
—
—
—
—
—
—
Nth
–0.05*
–0.05*
–0.07*
–0.02*
–0.06*
–0.05*
–0.05*
0.40
1.00
—
—
—
—
—
—
—
—
—
—
CI
–0.08*
0.20*
–0.02*
0.19*
0.17*
0.18*
0.14*
1.00
—
—
—
—
—
—
—
—
—
—
—
D
MCD
MCA
0.16*
0.11*
0.58
0.70
0.38*†
0.04*
0.93
0.15*
0.23*†
1.00
—
—
—
—
—
—
—
—
—
—
—
—
—
—
0.86
0.88
1.00
—
—
—
—
—
—
—
—
—
—
—
—
—
0.02*
0.80
0.91
0.62
1.00
—
—
—
—
—
—
—
—
—
—
—
—
MCL
Table 4. Correlation coefficient matrix comparing variables among crown portions for red pine (Pinus resinosa) on Black Island, Manitoba (n = 240).
MFM
0.18*
0.56
0.29*†
1.00
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
MSM
0.53
–0.04*
1.00
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
MSC
0.19*
1.00
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
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489
Table 5. Basic statistics of variables measured for comparison among cones and seeds of red pine (Pinus
resinosa) on Black Island, Manitoba.
Variable
n
Minimum
Maximum
Mean
Cone length (mm)
Cone diameter (mm)
Cone fresh mass (g)
Mean seed mass (g × 10–2)
Total seeds per cone
Mean seed length (mm)
Mean seed diameter (mm)
Mean seed area (mm)
% germination
5 days
10 days
15 days
20 days
25 days
30 days
503
503
503
477
476
476
476
476
32.61
19.37
5.75
0.47
7
3.81
2.26
6.39
59.83
32.86
23.97
1.18
88
4.70
2.88
9.38
48.61
27.47
13.88
0.83
53.26
4.26
2.57
7.85
SD
3.86
2.00
2.72
0.10
13.02
0.17
0.10
0.57
467
466
467
468
468
468
0
0
40
43.33
43.33
43.33
3.33
100
100
100
100
100
0.02
53.61
89.04
89.72
90.58
90.92
0.27
36.36
10.71
10.44
10.09
9.85
Results
Comparisons among trees
The 60 sampled trees had an average diameter of 20 cm
and were 11 m tall and about 51 years old (Table 1). The total number of cones per tree ranged from 0 to 256. Pearson
correlations revealed that older trees were significantly
taller, had smaller basal area increments, and had a higher
competition index (Table 2). The total number of cones produced per tree was significantly and positively correlated
with tree diameter, basal area increments (1–4 years before
cone maturation), and crown area. The basal area increment
for 2000 was not significantly correlated with total cone
number. The competition index was negatively correlated
with the number of cones (Table 2). Cone characteristics (diameter, length, number of seeds) and seed characteristics
(size, germination success) were not significantly correlated
with the variables measured at the tree level.
At the tree level, a multiple regression using backward selection showed that cone production was best predicted by
tree diameter and mean distance (four portions) to the neighbour tree (total number of cones = (11.37 × dbh) + (9.32 ×
mean distance) – 235.61). More cones were thus produced
by larger trees growing in a more open environment. The regression model was highly significant and explained 52% of
the variance (adjusted R2).
Comparisons among crown portions
The 240 crown portion areas varied between 1 and 20 m2
with an average of 10.76 m2 (Table 3). The number of cones
per crown portion varied from 0 to 82 and the competition
index from 21.60 to 81.22% (Table 3). Pearson correlation
coefficients indicate that crown portion area was most highly
correlated with the length of the longest living branch followed by bole length and lowest living branch height (Table 4). Crown portions with a high competition index value
also had lowest living branches higher on the stem, a smaller
value for the longest living branch, and a smaller crown portion area. The total number of cones per crown portion was
significantly and positively correlated with the longest living
branch length, bole length, crown portion area, and nearest
neighbour tree distance (Table 4). As for the tree level, cone
characteristics (diameter, length, number of seeds) and seed
characteristics (size, germination success) were not significantly correlated with variables measured in the field at the
crown portion level.
When comparing crown portions, a multiple regression
using backward selection shows that cone production is best
predicted by crown portion area, nearest neighbour tree diameter, and competition index (total number of cones =
(0.92 × crown area) + (0.38 × nearest neighbour tree diameter) + (–0.50 × competition index) + 18.50). More cones
were produced on larger crown portions in more open sites.
The regression model was highly significant and explained
20.4% of the variance (adjusted R2).
Comparisons among cones
Cone sizes for red pine averaged 48.61 × 27.47 mm with
a mean fresh mass of about 13.88 g (Table 5). These three
variables are significantly and strongly correlated as indicated by the results from the regression analysis (Fig. 2).
Mean seed mass for all cones was 0.83 g per 100 seeds with
a mean number of 53 seeds per cone (Table 5). Germination
tests yielded high germination success of more than 89%
germination after 15 days. At least 40% of seeds germinated
from any cone tested (Table 5).
Pearson correlations indicate that seed characteristics
(number of seeds per cone, mean and total seed mass per
cone, seed size parameters) are significantly and positively
correlated with cone characteristics (length, diameter, area,
fresh mass) (Table 6). Cone diameter is the cone size variable most strongly correlated with the total number and total
mass of seeds per cone. Of all of the variables measured,
only the mean seed mass and total seed mass are significantly and positively correlated with germination success after 30 days (Table 6). This is further illustrated by the
second-order polynomial regression between mean seed
mass and percent germination (Fig. 3). From this analysis, a
threshold value was apparent where increasing mean seed
mass was no longer a factor in increasing germination success (Fig. 3).
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Can. J. Bot. Vol. 80, 2002
Table 6. Correlation coefficient matrix comparing variables among cone and seeds of red pine (Pinus resinosa) on Black Island, Manitoba (n > 450).
Variable
CL
CD
CA
CFM
MSM
S/C
TSM
SL
SD
SA
%G
Cone length (CL)
Cone diameter (CD)
Cone area (CA)
Cone fresh mass (CFM)
Mean seed mass (MSM)
Total seeds per cone (S/C)
Total seed mass (TSM)
Seed length (SL)
Seed diameter (SD)
Seed area (SA)
Germination success (30 days) (%G)
1.00
0.73
0.94
0.86
0.28
0.52
0.59
0.48
0.29
0.38
0.03*
—
1.00
0.92
0.90
0.35
0.73
0.80
0.37
0.20
0.27
0.10*†
—
—
1.00
0.95
0.34
0.66
0.74
0.46
0.27
0.35
0.07*
—
—
—
1.00
0.41
0.63
0.75
0.49
0.35
0.41
0.11*†
—
—
—
—
1.00
0.02*
0.43
0.69
0.77
0.75
0.58
—
—
—
—
—
1.00
0.91
–0.10*†
–0.22
–0.22
0.15
—
—
—
—
—
—
1.00
0.19
0.12*†
0.11*†
0.37
—
—
—
—
—
—
—
1.00
0.78
0.94
0.07*
—
—
—
—
—
—
—
—
1.00
0.94
0.16
—
—
—
—
—
—
—
—
—
1.00
0.07*
—
—
—
—
—
—
—
—
—
—
1.00
*Not significantly correlated; all others values were significant at p = 0.05 after a Bonferroni correction.
†
Values significant at p = 0.05 with uncorrected probability but not with Bonferroni correction.
Fig. 3. Relationship between seed mass and percent germination
for red pine (Pinus resinosa) on Black Island, Manitoba. The
regression equations are provided along with R2 and n values.
The relationship is significant at p < 0.0001.
Discussion
Our results showed that the general statement that populations of red pine at the northern edge of its range are poor
cone producers and have reduced seed production (Fraser
1951; Cayford 1964; Rudolf 1965, 1990; Stiell 1988;
Bergeron and Brisson 1990; Sims et al. 1990) does not apply
to the most northerly and westerly occurrence of the species
in North America, at least for the year 2000. In southeastern
Manitoba, cone production in 2000 was generally good but
not considered to have been exceptional. Cone production
varied across the region, with some areas having no cone
production (David Flight, personal communication). On
Black Island, trees produced “no cones” to “moderate crops”
according to the definitions of Schooley et al. (1986). The
number of cones produced per tree was between 50 and 200,
i.e., within the range described by Sims et al. (1990). In addition, field observations from 1999 to 2001 indicate that red
pine trees produced cones during 3 successive years.
Our results also indicated that reproduction characteristics
of red pine on Black Island were well within the normal
range of production, size, and viability for the species. The
average length of cones was found to be within the range of
4–5 cm (Lyons 1956; Rudolf 1965, 1990; Dickmann and
Kozlowski 1969b; Sims et al. 1990; Keeley and Zedler
1998). These previous studies found that the average number
of seeds in red pine cones is approximately 45, compared
with an average of 53 seeds per cone in this study. Germination success in this study was well above the 14–65% value
reported by Sims et al. (1990). Numbers were comparable
with those of Cayford (1964) who obtained 86 and 67% germination in the 1957 and 1960 seed crops, respectively, from
the Sandilands Forest Reserve in southeastern Manitoba.
Under laboratory conditions, Flannigan and Woodward
(1993) also obtained germination success in the order of 80–
90%. Similar numbers were also obtained during field trials
at the northern limit of the species’ distribution range
(Flannigan and Bergeron 1998). Butson et al. (1987) and
Roberts (1989) also found red pine seed to be viable at the
limit of its distribution. Our results support those of
Flannigan and Bergeron (1998) who concluded that seed
germination and cone and seed production are not responsible for the northern distribution limit of red pine. Stevens
and Enquist (1998) observed that seed size and size of current geographical range in Pinus are not correlated.
Comparisons among trees
Of the variables measured for individual trees, number of
cones was found to be significantly related to dbh and to
nearest neighbour distance. This means that larger trees and
those that were more distant from the nearest neighbours
produced more cones. This suggested that light availability
played an important role in influencing the production of
cones. Stiell (1988) observed that red pine trees with larger
dbh values generally produce more cones than smaller ones.
Stiell (1971) observed that for a similar dbh, wider spacing
was associated with more cones. Rudolf (1990) and Sims et
al. (1990) also mentioned that trees in overstocked stands
have very low seed fall, and many trees do not produce
cones because of excess shading.
Correlation analyses indicate that the more productive
trees were those with wider basal area increments before
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Sutton et al.
cone primordia initiation (1996–1997), during the year of
cone primordia initiation (1998), and during the year of cone
emergence and pollination (1999). This suggested that cone
production could be enhanced during years of increased radial growth, i.e., when larger reserves are accumulated by
the tree. For 2000, however, basal area increment is not significantly correlated with cone abundance. This strongly
suggests that during the year of cone maturation, a portion
of the energy normally allocated to radial growth was diverted to cone development. During the year of maturation,
cones of red pine acquire 67 and 97.5% of their final length
and mass, respectively (Lyons 1956; Dickmann and
Kozlowski 1969b). Considerable energy is needed to accomplish this growth, and although the cones were able to photosynthesize (Dickmann and Kozlowski 1970), they
depended mostly on other sources for nutrition. Others have
suggested that cone and seed production reduce vegetative
growth (Eis et al. 1965; Kozlowski 1971; Harper 1977; Wilson 1983; Fenner 1985; Barnes et al. 1998; Keeley and
Zedler 1998). This occurs because the vegetative parts of the
tree receive less photosynthates, which are instead directed
into the cones. Developing cones are major resource sinks,
as they depend largely on needle and stem reserves and current photosynthates from 1-year-old needles (Dickmann and
Kozlowski 1968; Kozlowski 1971; Wilson 1983; Barnes et
al. 1998).
Comparisons among crown portions
Contrary to our expectations, cone, seed, and germination
characteristics were not correlated with the sizes of individual crown portions. It was hypothesized that larger crown
portions would have higher photosynthetic reserves to allocate to the cones and that this would influence both cone
size and seed size. Our results showed that crown portion
size solely influenced cone abundance. We speculated that
compared with small crown portions, large crown portions
maintain more cones instead of larger cones. Cone size may
depend more on the success of fertilization and the ultimate
number of seeds that will develop. In the case of seed size,
even though it is known to be at least partly related to parent
plant size, phenotypically it is one of the characteristics that
is the least affected by environmental factors (Harper 1977;
Fenner 1985).
When comparing crown portions, the variables influencing cone abundance were mainly bole length, crown portion
area, and nearest tree distance. These factors are all related
in some way to competition for light. Neighbouring plants
can reduce light received by an individual through interception (Harper 1977). Stiell (1988) also found that trees with
larger dbh and larger crown surface produce most of the
cone crop of a stand.
Comparisons among cones
Cone size variability, which showed no correlation with
any of the tree and crown portion characteristics, was related
to cone characteristics. Cone size and the number of seeds
per cone were found to be positively correlated, i.e., larger
cones contained more seeds than smaller ones. In addition,
we found that larger, heavier cones also contained larger
seeds. Although Lyons (1956) stated that seed yield varies
directly with cone length, our data indicate that cone width
491
is a better estimator of seed yield. Even though it is a reproductive strategy of some plants to partition their output into
either few large seeds or many small seeds (Fenner 1985),
our results show that seed number and size increased with
cone size. Caron and Powell (1989) found similar significant
correlations between total seed number per cone and cone
length and mass in black spruce plantation trees in northwestern New Brunswick. It would seem that cone size depends largely on pollination and fertilization success, which
dictates the number of seeds that will grow and mature
(Fenner 1985). Pollination success is also largely dependent
on weather conditions (Barnes et al. 1998).
Our results strongly suggest that seed mass positively affected germination success up to a threshold value. Above
this value, seed mass may determine survival after germination, but this remains unknown. Horton and Bedell (1960)
reported that seed mass in eastern white pine (Pinus
strobus L.) and red pine is an important factor for germination success. Houle and Filion (1993) found a positive, significant correlation between seed mass and germination rate
for one of their jack pine populations but not for the other.
They proposed that the heavier seeds of jack pine germinate
faster and the resulting seedlings have a better chance of survival in a relatively short growing season at the northern
limit of the species’ distribution range. Seed size is an index
of the material and energetic investment from the parent
plant into the offspring (Harper 1977; Wilson 1983). It is evident, therefore, that one of the most effective adaptations
for ensuring successful seedling establishment is the possession of a large seed that contains large reserves of nutrients
for survival of the seedling in the period following germination (Wilson 1983; Fenner 1985). Venable and Brown (1988)
also reported that, in general, seed mass is an important factor for germination success in most species and that larger
seeds also tend to be better prepared for survival after germination because of their larger store of reserves. Spurr (1944)
observed that seed mass influences germination rate in white
pine, that seeds with lower masses do not germinate, and
that heavy seeds germinate faster than light seeds. Seedlings
from heavier seeds are significantly larger in white pine, experience a longer growing season, and survive longer than
seedlings from lighter, smaller seeds (Spurr 1944).
The existence of a threshold value requires further evidence, since only 63 of the 479 cones had germination success lower than 85%. Perhaps cones with less than 85%
germination were not as mature as the other ones. The 63
cones came from 17 of the 60 sample trees. Among these 17
trees, one tree, even though it had many cones (28 in total),
only had one cone with a germination success higher than
85%. This tree was a geographic outlier, being the farthest
west of any of the sample trees, possibly making pollination
less effective. Smith et al. (1988) suggested that although
open-grown, semi-isolated individuals may often produce
abundant and easily collected cones, many seeds are inviable
because of higher rates of self-fertilization in such situations.
Conclusion
The influence of ecological factors on the reproductive
ecology of red pine has been assessed for trees growing at
the northwest limit of their distribution range. Our data do
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492
not confirm previous statements that red pine at the northern
limit of the species distribution produce less cones, less
seeds, or seeds with lower germination success than more
central populations. Several factors influenced the reproduction of red pine. Cone abundance was influenced more
strongly by tree size than by age. The number of cones per
crown portion was found to be a function of competition for
light. Both tree and crown portion characteristics did not,
however, influence the characteristics of the individual
cones or seeds or germination success. After cone initiation
and fertilization, the growth of the cones and seeds did not
appear to be influenced by the amount of light reaching the
crown or the amount of photosynthesis done by the crown.
Results show that cone size is a function of the number of
seeds that develop in the cone and the size of those seeds.
Larger cones contained more and larger seeds than smaller
ones. Germination success was also a function of seed size.
The relationship between seed mass and germination success
suggests that there was a threshold where seed mass became
less important, and we hypothesize that larger size will give
the developing seedling a greater chance at survival.
Acknowledgements
This study was conducted as part of the requirements for
an honours degree in biology by the first author. We thank
D. Bailey, L. Buchanan, F. Conciatori, G. Damiani, D.
Flight, J. Joa, K. Jones, and K. Skibo for their field and (or)
laboratory assistance. We also thank the two anonymous reviewers and the Associate Editor for their constructive comments. We thank Manitoba Hydro (Forest Enhancement
Program), the Natural Sciences and Engineering Research
Council of Canada, Manitoba Conservation, and the University of Winnipeg for their financial and (or) logistic support.
We are also grateful to the Hollow Water First Nation for
their cooperation and for giving us the opportunity to appreciate Black Island.
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