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Demography of the columnar cactus Neobuxbaumia macrocephala: A

comparative approach using population projection matrices

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 Plant Ecology 174: 109–118, 2004. 109
© 2004 Kluwer Academic Publishers. Printed in the Netherlands.

Demography of the columnar cactus Neobuxbaumia macrocephala: a

comparative approach using population projection matrices

Héctor Godínez-Alvarez1,2,* and Alfonso Valiente-Banuet1

1
Instituto de Ecología, Universidad Nacional Autónoma de México, Apartado Postal 70-275. Coyoacán C. P.
04510, México, D. F.; 2UBIPRO, FES-Iztacala, UNAM. Av. de los Barrios 1, Los Reyes Iztacala, Tlalnepantla
54090, Ap. Postal 314, Edo. de Mexico, Mexico; *Author for correspondence (tel.: 56-23-12-28; fax
56-23-12-25; e-mail: chanogod@yahoo.com)

Received 20 November 2002; accepted in revised form 9 July 2003

Key words: Cactaceae, Fecundity, Pollen limitation, Rarity, Recruitment, Tehuacán Valley

Abstract

Neobuxbaumia macrocephala is a long-lived columnar cactus endemic to the Tehuacán-Cuicatlán Valley in

south-central Mexico. This plant has a very restricted distribution and few recruitment events have been detected
in its populations. In this study, we analyze the N. macrocephala demographic pattern using a projection matrix
in order to determine the main limiting factors of this species. To accomplish this goal, we compare our results
with those obtained for another species of the same genus, N. tetetzo. Considering that both species inhabit the
same valley, we believe that this comparative study will offer insights into the main demographic limitations of
N. macrocephala. Results showed that these species of columnar cacti have similar demographic patterns in which
survival is the process with the highest relative contribution to ␭, followed by growth and reproduction. Of all
the life cycle stages, seeds and seedlings have the lowest survival probabilities due to a high mortality caused by
seed predation and effects of direct solar radiation on germinated seeds. The estimated growth rates indicate that
populations of these species of Neobuxbaumia are in a numerical equilibrium. With respect to reproduction, N.
macrocephala produce a lower number of seeds per plant than N. tetetzo. This low level of sexual reproduction
may decrease the probability of establishment of new individuals in N. macrocephala populations. It is suggested
that pollen limitation and pre-dispersal seed predation could be some factors that limit the distribution and abun-
dance of this columnar cactus.

Introduction Fiedler 1987; Byers and Meagher 1997; Silva et al.

One of the major goals in ecological studies is to de-
termine the factors that limit the distribution and
abundance of rare species of plants 共Kruckeberg and
Rabinowitz 1985; Gaston 1994兲. In this regard, com-
parative demographic studies of closely-related rare
and common species represent a useful approach in
the understanding of these factors. Comparative stud-
ies of related species could provide information on
the way in which some biotic and abiotic factors dif-
ferently affect plants with very contrasting abun-
dances and range distributions 共Angevine 1983;
2000兲.
Matrix models along with elasticity analyses con-
tribute significantly to the accomplishment of these
comparative studies by providing basic demographic
information on populations 共Caswell 1989兲. Matrix
models yield measures of structure and behavior such
as the growth rate, the stable size distribution, and the
reproductive values whereas elasticity analyses allow
the identification of the life cycle stages that have the
greatest effect on the population growth 共Caswell
1989; Silvertown et al. 1993; Schemske et al. 1994兲.
Information obtained in these analyses would facili-
110
tate the comparison of congeneric species and, at the
same time, offer insights into the main ecological
factors that affect persistence of plants.
Columnar cacti inhabiting North American deserts
are a group of plants in which sparse and common
species exist 共Godínez-Alvarez et al. in press兲. These
plants represent an excellent opportunity to conduct
comparative studies in order to determine the factors
that affect the abundance and distribution of rare spe-
cies. Despite this fact, at present, no work with this
approach has been conducted probably because data
necessary to construct projection matrices is difficult
to obtain for long-lived plants. This paper analyzes
the demography of two columnar cacti of the genus
Neobuxbaumia, which is endemic to the Tehuacán-
Cuicatlán Valley in south-central Mexico 共Valiente-
Banuet et al. 2000兲. Neobuxbaumia tetetzo 共Coulter兲
Backeberg is an abundant species averaging 1200 in-
dividuals per hectare that occupies hundreds of square
kilometers at 1500–1700 m a. s. l. 共Valiente-Banuet
et al. 2000兲. On the other hand, Neobuxbaumia mac-
rocephala Weber 共Dawson兲 is a species with a
remarkably limited distribution restricted to small ar-
eas ca. 1700 m a. s. l., in the western part of the Te-
huacán-Cuicatlán Valley. Field observations have
indicated that N. tetetzo populations show a higher
number of seedlings over a wider distribution area
than N. macrocephala populations which occur in
patches with low densities and recruitment events,
suggesting that this last species faces ecological limi-
tations for population growth. Considering the previ-
ous information, we believe that the demographic
analysis of N. macrocephala and its comparison with
the common species, N. tetetzo, will offer insights
into the main factors limiting the distribution and
abundance of this species. In this regard, a previous
study conducted with N. macrocephala 共Esparza-
Olguín et al. 2002兲 found that ␭ increases signifi-
cantly when either fecundity or seedling survival
probability were increased 10-fold, indicating that a
low reproductive potential might be contributing sig-
nificantly to its rarity in the Tehuacán Valley.
In this study, we use projection matrices in order
to obtain the growth rate and the stable size distribu-
tion of a population of N. macrocephala, not consid-
ered by Esparza-Olguín et al. 共2002兲. Further, we
conduct an elasticity analysis to determine the rela-
tive importance of survival, growth, and fecundity to
␭. Specifically, we address the following questions: 1兲
Does the population of N. macrocephala have a stable
size distribution?; 2兲 What is the growth rate of the
N. macrocephala population?; 3兲 What are the rela-
tive contributions of survival, growth, and fecundity
to the population growth of N. macrocephala?; 4兲 Are
N. macrocephala seeds and seedlings the life cycle
stages with the highest mortality?; 5兲 What are the
main mortality factors of these life cycle stages?; and
6兲 Do the demographic differences found between
these two columnar cacti account for the observed
rarity of N. macrocephala relative to N. tetetzo?
Methods
Study site and natural history of Neobuxbaumia
macrocephala
The study was conducted in the semiarid Valley of
Zapotitlán 共18°20' N, 97°28' W兲, a local basin of the
Tehuacán-Cuicatlán Valley in the state of Puebla,
Mexico. This region owes its aridity to the rain
shadow produced by the Eastern Sierra Madre 共Smith
1965兲. It has an average rainfall of 380 mm and an
annual mean temperature of 21 °C with rare frosts
共García 1973兲. The main vegetation type is an arid
tropical scrub in which columnar cacti are dominant
elements of the vegetation 共Valiente-Banuet et al.
2000兲.
N. macrocephala is a branched columnar cactus
that reaches 10 m in height with densities of 200 in-
dividuals/ha 共Valiente-Banuet et al. 1997兲. Seed ger-
mination and seedling establishment occurs mostly
beneath the canopies of several species of trees and
shrubs, such as Pseudosmodingium multifolium Rose,
Lippia graveolens Knuth, Gochnatia hypoleuca 共DC.兲
A. Gray, and Aeschynomene compacta Rose. First re-
production occurs when plants are around 2 m tall
共Valiente-Banuet et al. 1997兲. Flowering occurs from
March to June whereas fruiting occurs from July to
August. The species is hermaphroditic and its flowers
are mainly nocturnal, opening at sunset 共1900 h兲 and
closing in the morning 共1000 h兲. The bats Choeronyc-
teris mexicana Tschudi, Leptonycteris curasoae
Miller, and Leptonycteris nivalis 共Saussure兲 are the
main pollinators that promote seed production 共Va-
liente-Banuet et al. 1997兲. These bats also consume
the pulp and seeds of fruits, acting probably as seed
dispersers 共Valiente-Banuet et al. 1997兲.

The demographic model
In order to determine the main demographic traits of
N. macrocephala, we constructed a matrix model
共Caswell 1989兲. This model consists basically of a
projection matrix 共A兲 and a vector 共v兲. The A matrix
is composed of three principal parts: 1兲 the first row
gives fecundity values for all reproductive size cat-
egories; 2兲 the principal diagonal defines probabilities
of stasis, or proportions of individuals in size
category i that remain in the same category after one
time interval; and 3兲 the first sub-diagonal defines
transition probabilities, or proportion of individuals in
size category i that grow to the next category. The v
vector defines the number of individuals in the popu-
lation for each size category at time t. When the ma-
trix A is post-multiplied by the vector v one can
obtain the population vector at time t+1. If this ma-
trix multiplication is repeated over several time-steps,
the proportions of individuals belonging to different
size categories will become constant 共i.e., stable size
distribution兲 and the population will grow, remain
stable, or decline at a constant rate 共i.e., finite rate of
increase or ␭兲. The assumptions of this matrix model,
in order to provide valid projections, are that transi-
tion probabilities remain constant over time and inde-
pendent of population density 共Caswell 1989兲.
Additionally, with the stable size distribution and
the reproductive values an elasticity analysis could be
performed to determine the most critical stages of the
life cycle. Elasticity is a measure of the relative
change in the population finite rate of increase in re-
sponse to small changes in the value of a matrix ele-
ment 共de Kroon et al. 1986兲.
Field methods
During the dry season in April and May of 1996, a
total of 250 individuals of N. macrocephala were
tagged and the height of the principal trunk was mea-
sured with a leveling rod. Size categories were deter-
mined following ontogenetic stages and association
with nurse plants as follows: 0–15 cm ⫽ Seedling;
15–45 cm ⫽ Sapling; 45–100 cm ⫽ Juvenile; 100–
150 cm ⫽ Immature; 150–250 cm ⫽ Mature 1; 250–
350 cm ⫽ Mature 2; 350–450 cm ⫽ Mature 3; 450–
550 cm ⫽ Mature 4; 550–650 cm ⫽ Mature 5; ⱖ
650 cm ⫽ Mature 6. Size categories of seedling, sap-
ling, juvenile, immature and mature 1 are mostly as-
sociated with nurse plants, whereas the other mature
categories grow isolated with respect to trees and
111
shrubs 共H. Godínez-Alvarez, pers. obs兲. Mature 1
category includes individuals that reached the first re-
production event, although they presented very low
reproduction probabilities. In 1997 and 1998, new
censuses were conducted in order to determine the
annual height increments.
The number of fruits produced per plant was
recorded during the fruiting seasons of 1997 and
1998. Additionally, a random sample of fruits 共n ⫽
27兲 was collected in 1998 to estimate the mean num-
ber of seeds per fruit. For all the individuals ⱖ 200
cm in height, the probability of reproduction was ob-
tained as the proportion of individuals that produced
fruits. These data were used to calculate fecundity
values as detailed later.
Estimations of seed germination and seedling sur-
vivorship were obtained experimentally in the study
area. With this experiment, it was possible to deter-
mine the survivorship of N. macrocephala seeds and
seedlings in different environmental conditions as
well as to estimate the transition probabilities of these
life cycle stages. The treatments followed a 2 ⫻ 2 fac-
torial design in which seeds of N. macrocephala were
sown in open spaces and beneath the canopy of the
most common nurse plant in the study zone,
Pseudosmodingium multifolium, in sites in which
predators were either excluded or non-excluded.
Seeds were obtained from ripe, open fruits and the
fleshy mesocarp was dried and removed before sow-
ing. Each experimental unit consisted of 100 seeds
sown in a 30 ⫻ 30 cm plot and 5 replicates were per-
formed for each treatment. The soil surface was
cleaned of other seeds and cactus seedlings and the
seeds were sown directly on the surface. Rodents and
birds were excluded by completely covering the ex-
perimental unit with a 12 mm wire mesh with the
bottom edges buried in the soil. Ants were excluded
using a chlorate insecticide powder 共‘Ant-Stop’兲 and
a natural resin 共‘Tangle Foot’兲. Seed germination was
evaluated considering the maximum number of
emerged seedlings per treatment. Additionally, treat-
ments were checked approximately every 20–30 days
from July 1998 to July 1999 to count the number of
surviving seedlings in each replicate.
Data analysis
Differences in seed germination were analyzed
through a contingency table made with a log-linear
model 共Crawley 1993兲. The null hypothesis was that
there were an equal number of emerged seedlings in
112
each treatment. Similarly, seedling survivorship was
analyzed using log-linear models in which time was
a continuous variable and treatments were categorical
variables. The models were fitted following Valiente-
Banuet and Ezcurra 共1991兲 and using the GLIM sta-
tistical package version 3.77 共Crawley 1993兲. Accord-
ing to Valiente-Banuet and Ezcurra 共1991兲, mortality
rates that change through time could be described by
the equation 1/N · dN/dt = – d + bt, where d is the
initial mortality rate at time t ⫽ 0, and b is a param-
eter that describes whether the initial rate increases or
decreases. The integration of this equation results in
Nt = exp(a – dt + ct2) where Nt is the number of sur-
vivors at time t, a ⫽ ln N0, and c ⫽ b/2. The param-
eter c represents the intensity with which mortality
rates varied in time. If c ⬍ 0, the model describes a
type I survivorship curve whereas if c ⬎ 0, the survi-
vorship curve is type III.
In order to construct the matrix model, stasis and
transition probabilities among size categories were
estimated by calculating the proportion of individuals
that remained in the same category or passed from
one category to the next in one year. With respect to
fecundities, these were calculated as the product of
the probability of reproduction, the mean number of
fruits per plant, the mean number of seeds per fruit
共627 ⫾ 25, n ⫽ 27; hereafter, data will be reported
as mean ⫾ standard error unless otherwise stated兲,
and the probability of passing from seed to seedling.
In turn, the probability of passing from seed to seed-
ling was calculated multiplying the number of survi-
vors after one year beneath the canopy of P.
multifolium in the non-excluded treatment 共0.002,
given by the results of the seed germination and
seedling survivorship experiment兲 by the proportion
of soil covered by shrubs 共76%兲. Fecundities were
calculated in this manner because N. macrocephala
seeds germinate during the rainy season of the same
year and no seed bank has been detected.
With stasis and transition probabilities as well as
fecundity values for both years, 1997 and 1998, an
average projection matrix was constructed and
iterated to estimate ␭ and the stable size distribution.
The stable size distribution predicted by the model
was compared to the actual distribution of individu-
als in size categories using a G test 共Sokal and Rohlf
1981兲.
Confidence limits 共95%兲 for ␭ were calculated
through Monte Carlo simulation models 共Alvarez-
Buylla and Slatkin 1993兲. The variances for all the
matrix entries were estimated assuming a log-normal
distribution of errors for fecundity values and a mul-
tinomial distribution of errors for transition probabili-
ties. With these assumptions, 1000 simulations were
run and the sampling distribution of ␭ was con-
structed. Confidence limits were determined consid-
ering the values of the 2.5 and 97.5 percentiles.
Elasticity values were obtained to determine the
contribution of each matrix entry to ␭. Additionally,
we estimated the relative contributions of survival,
growth, and fecundity to the finite rate of increase
following the methodology proposed by Silvertown et
al. 共1993兲.
All parameters 共i.e., ␭, stable size distribution,
confidence limits, and elasticity values兲 were obtained
using a program especially designed for this purpose
written in the programming language Pascal.
Comparison of N. macrocephala and N. tetetzo
The results obtained for N. macrocephala were com-
pared to those reported for its related species N. te-
tetzo 共Godínez-Alvarez et al. 1999兲. This comparison
was made considering measures of structure and be-
havior of the populations such as ␭, size-frequency
distributions, and elasticities. However, to accomplish
this goal it was necessary to consider firstly the num-
ber of categories used in the construction of the ma-
trix models for both species, since they affect the
estimation of the transition probabilities 共Caswell
1989, Silvertown et al. 1993兲. Originally, the life
cycle of N. tetetzo was divided in twelve categories
共Godínez-Alvarez et al. 1999兲 whereas the number of
categories used in this study for N. macrocephala was
ten. Therefore, with the raw data of N. tetetzo a new
projection matrix was constructed in which the size
categories were similar to those used for N. macro-
cephala. With this new projection matrix, ␭ and its
95% confidence limits, as well as the elasticity val-
ues, were calculated for N. tetetzo in the same man-
ner as detailed above for N. macrocephala.
The stasis and transition probabilities of the
projection matrices constructed for N. macrocephala
and N. tetetzo were compared using a log-linear
model with conditional independence in which the
effect of species on the state and/or fate of individu-
als was estimated 共Caswell 1989兲. Additionally, the
number of seeds produced per plant for both species
was compared with a log-linear model in which spe-
cies and reproductive categories were considered as
categorical variables. These models were fitted using

GLIM release 4 and JMP version 3.1 共SAS 1995兲, re-
spectively.
The comparison of N. macrocephala and N. tetetzo
population rates of increase was made considering the
95% confidence limits. Moreover, the actual size dis-
tributions of both species were compared using a G
test 共Sokal and Rohlf 1981兲.
Elasticity values of N. macrocephala and N. tetetzo
were compared calculating the relative contributions
of growth 共G兲, survival 共L兲, and fecundity 共F兲 to ␭
according to Silvertown et al. 共1993兲.
Results
Seedling emergence and survival
The maximum number of emerged seedlings in all
treatments was reached after 100 days of the begin-
ning of the experiment. Emergence varied among
treatments, obtaining the highest number of seedlings
under the shade of P. multifolium and excluded from
predators 共20 ⫾ 9, n ⫽ 5, range 0–49兲 whereas the
lowest was obtained in open spaces and excluded
from predators 共0.8 ⫾ 0.4, n ⫽ 5, range 0–2兲. In
open spaces exposed to the action of predators, seed
germination did not occur because of the predation of
seeds by the ant Crematogaster opaca Mayr. The
analysis of deviance for the number of emerged seed-
lings showed that the effects of predators 共G ⫽ 8.02,
d. f. ⫽ 1, p ⫽ 0.005兲 and shade 共G ⫽ 14.52, d. f. ⫽
1, p ⫽ 0.0001兲 were significant, but not their interac-
tion 共G ⫽ 0.13, d. f. ⫽ 1, p ⫽ 0.723兲. The proportion
of variance explained by these two factors, predation
and shade, were 21% and 38% respectively.
After 336 days, only those treatments located be-
neath the canopies of P. multifolium in sites in which
predators were either excluded 共14 ⫾ 9, n ⫽ 5, range
0–47兲 or non-excluded 共0.2 ⫾ 0.2, n ⫽ 5, range 0–1兲
had surviving seedlings. In contrast, seedlings in the
other treatments died 236 days after the beginning of
the experiment. The analysis of the survivorship
curves showed that time explained 88% of the total
variance whereas the interaction between treatment
and time explained 5%. The initial mortality rates
varied among treatments. The lowest and highest
rates were estimated under P. multifolium with preda-
tors excluded 共-0.034 ⫾ 0.003兲 and in open spaces
with predators excluded 共-0.058 ⫾ 0.008兲, respec-
tively. The intensity of change in mortality rates 共pa-
rameter c兲 was positive 共0.0000737兲 and significantly
113
different from zero 共t ⫽ 7.7, d. f. ⫽ 85, p ⬍ 0.0005兲
which indicates that all survivorship curves are type
III.
Finite rate of increase and stable size distribution
Seeds presented the lowest survival probability
because only 1 of 500 seedlings was alive in non-ex-
cluded treatments under P. multifolium at the end of
the experiment. On the other hand, survival probabil-
ities increased for the rest of the size categories 共Table
1a兲. The proportion of individuals that changed from
one category to the next after a 1-year period was low
ranging, from 1% for seedlings and mature 4
individuals to 19% for immature individuals. Fecun-
dity was higher for mature 4 and mature 6 individu-
als and decreased for the rest of the reproductive
categories. In general, fecundities increased with size
共Table 1a兲. The estimated ␭ value was 1.05 with con-
fidence limits of 0.96 and 1.08, indicating that it was
not different from unity.
The size structure observed in the field showed that
there are two peaks that concentrate a high propor-
tion of individuals 共Figure 1兲. In the first peak, indi-
viduals of the juvenile, immature and mature 1
categories represent approximately 59% of the popu-
lation whereas in the second peak, individuals of the
mature 5 category constitute 10% of the total. The
proportion of individuals for the rest of the categories
was low, representing only 31%. This actual distribu-
tion differs significantly from the stable size distribu-
tion predicted by the model 共G ⫽ 579.8, d. f. ⫽ 9, p
⬍ 0.00001兲. In the stable size distribution, the pro-
portion of individuals decreased with size 共Table 1a兲.
It is important to emphasize that differences
between the actual and predicted size distributions
indicate that our matrix model does not represent well
the dynamics of the population studied. Thus, the es-
timation of the finite rate of increase and the elastic-
ity analysis results should be interpreted with caution.
Elasticity analysis
Elasticities showed that there were differences among
the size categories in the relative contribution to ␭.
The category with the highest contribution was ma-
ture 4 whereas mature 5 and mature 6 were the cat-
egories with the lowest contribution 共Table 2a兲. When
we added up all the matrix entries to determine the
relative contribution of the main demographic pro-
cesses 共i.e., survival, growth, and fecundity兲, we
114

Table 1. Projection matrices and stable size distributions 共W兲 of Neobuxbaumia macrocephala 共a兲 and N. tetetzo 共b兲 growing in the Tehuacán-
Cuicatlán Valley, Mexico. Se, seedling; sa, sapling; j, juvenile; im, immature; m1–m6, mature individuals
Size Categories 共Nt兲
Size Categories 共Nt⫹1兲 se sa j im m1 m2 m3 m4 m5 m6 W
共a兲
se 0.66 0.32 2.22 20.4 18.5 27.4 0.873
sa 0.01 0.84 0.041
j 0.13 0.84 0.026
im 0.15 0.80 0.015
m1 0.19 0.85 0.013
m2 0.14 0.83 0.008
m3 0.17 0.92 0.010
m4 0.09 0.99 0.013
m5 0.01 0.89 0.001
m6 0.11 0.99 0.001

共b兲
se 0.76 8.7 14.9 22.4 28.2 29.3 0.563
sa 0.07 0.89 0.210
j 0.09 0.92 0.120
im 0.07 0.96 0.072
m1 0.04 0.94 0.021
m2 0.06 0.93 0.008
m3 0.06 0.93 0.003
m4 0.06 0.95 0.002
m5 0.05 0.82 3.2 ⫻ 10–4
m6 0.11 0.95 2.7 ⫻ 10–4

Comparison of N. macrocephala and N. tetetzo

The comparison of the projection matrices con-

Figure 1. Proportion of individuals per size category of N. macro-
cephala 共closed bars兲 and N. tetetzo 共open bars兲 in the Tehuacán-
Cuicatlán Valley, Mexico. Se, seedling; sa, sapling; j, juvenile; im,
immature; m1–m6, mature individuals.
found that survival was the most important one 共84%兲
followed by growth 共14%兲 and fecundity 共2%兲.
structed for N. macrocephala and N. tetetzo showed
that species does not have a significant effect 共␹2 ⫽
0.24, d. f. ⫽ 9, p ⬎ 0.05兲 on the state and/or fate of
individuals. This result indicates that transition prob-
abilities among the different categories are similar for
both species of columnar cacti 共Table 1兲.
The analysis of deviance for the number of seeds
produced per plant showed that the effects of species
共␹2 ⫽ 17.8, d. f. ⫽ 1, p ⬍ 0.00001兲 and reproduc-
tive categories 共␹2 ⫽ 34.6, d. f. ⫽ 3, p ⬍ 0.00001兲
were significant, but not their interaction 共␹2 ⫽ 7.02,
d. f. ⫽ 3, p ⫽ 0.071兲. The number of seeds produced
per plant is lower in N. macrocephala 共13.1 ⫻ 103 ⫾
1.5 ⫻ 103, n ⫽ 51, range 627 ⫺ 42.0 ⫻ 103兲 than in N.
tetetzo 共25.6 ⫻ 103 ⫾ 1.5 ⫻ 103, n ⫽ 249, range 552
⫺ 149.7 ⫻ 103兲. In both species, the first reproductive
categories had a lower number of seeds per plant
共Mature 3 ⫽ 15.2 ⫻ 103 ⫾ 1.5 ⫻ 103, n ⫽ 77, range
552 ⫺ 58.1 ⫻ 103兲 than the last ones 共Mature 6 ⫽
30.9 ⫻ 103 ⫾ 334, n ⫽ 73, range 1.7 ⫻ 103 ⫺
14.0 ⫻ 103; Figure 2兲. Besides differences in the num-
 115

Table 2. Elasticity matrices of Neobuxbaumia macrocephala 共a兲 and N. tetetzo 共b兲 growing in the Tehuacán-Cuicatlán Valley, Mexico. Se,
seedling; sa, sapling; j, juvenile; im, immature; m1–m6, mature individuals.
Size Categories 共Nt兲
Size Categories 共Nt⫹1兲 se sa j im m1 m2 m3 m4 m5 m6
共a兲
se 0.03 1.4 ⫻ 10–4 1.2 ⫻ 10–3 0.02 8.0 ⫻ 10–4 2.1 ⫻ 10–3
sa 0.02 0.07
j 0.02 0.08
im 0.02 0.06
m1 0.02 0.08
m2 0.02 0.07
m3 0.02 0.13
m4 0.02 0.28
m5 2.9 ⫻ 10–3 0.02
m6 2.1 ⫻ 10–3 0.03

共b兲
se 0.05 0.01 0.01 4.3 ⫻ 10–3 1.0 ⫻ 10–3 9.3 ⫻ 10–4
sa 0.02 0.10
j 0.02 0.12
im 0.02 0.17
m1 0.02 0.14
m2 0.02 0.13
m3 0.01 0.08
m4 0.01 0.05
m5 1.9 ⫻ 10–3 0.01
m6 9.3 ⫻ 10–4 0.01

The 95% confidence limits of ␭ 共0.96-1.08 for N.

Figure 2. Fecundity and probability of reproduction for N. macro-
cephala 共closed bars and symbols, respectively兲 and N. tetetzo
共open bars and symbols兲 growing in the Tehuacán-Cuicatlán Val-
ley, Mexico.
ber of seeds produced in each reproductive category,
the probability of reproduction for the mature
individuals varied according to species. In N. tetetzo,
the probability of reproduction was relatively con-
stant for all the reproductive categories whereas in N.
macrocephala it increased with size 共Figure 2兲.
macrocephala and 0.94-1.09 for N. tetetzo兲 showed
that the population growth rates estimated for N.
macrocephala 共1.05兲 and N. tetetzo 共1.07兲 did not
differ from unity, suggesting that populations of both
species are in a numerical equilibrium.
The actual size distribution of N. macrocephala
differed from the size distribution found for N. tetetzo
共G ⫽ 117.4, d. f. ⫽ 9, p ⬍ 0.00001兲, indicating that
these species varied in the number of individuals in
different size categories that constituted their popula-
tions. The population of N. macrocephala mostly
consisted of individuals in the pre-reproductive cat-
egories whereas seedlings were scarce. On the con-
trary, the population of N. tetetzo was characterized
by a high number of seedlings compared to the rest
of the categories in which the number of individuals
was low 共Figure 1兲.
The elasticity matrices showed that in both species
of Neobuxbaumia there were differences among the
size categories in the relative contribution to ␭ 共Table
2兲. Despite this fact, the addition of all the matrix en-
tries indicated that survival was the most important
life cycle component 共84% – N. macrocephala, 85%
116
– N. tetetzo兲 followed by growth 共14% – N. macro-
cephala, 13% – N. tetetzo兲 and fecundity 共2% – N.
macrocephala and N. tetetzo兲.
Discussion
The main purpose of this study was to compare the
demographic patterns of N. macrocephala and N. te-
tetzo in order to determine some of the factors that
limit the abundance and distribution of the former
species in the field. Our results indicate that both spe-
cies of columnar cacti have some similarities,
although there are differences in their reproductive
characteristics.
In general, both species of columnar cacti are
long-lived desert plants in which survival is the most
important component of the life cycle to ␭, followed
by growth and reproduction. Other species of colum-
nar cacti like Carnegiea gigantea 共Silvertown et al.
1993兲, Escontria chiotilla 共Ortega-Baes 2001兲, and
Pachycereus pringlei 共Silva 1996兲 have similar
demographic patterns. Survival of individuals in dif-
ferent size categories is essential for the persistence
of columnar cacti populations because they are slow-
growing plants with low transition and high stasis
probabilities 共Godínez-Alvarez et al. 1999兲. Matrix
analysis revealed that survival in N. macrocephala
increases according to plant height. Of all the life
cycle stages, seeds and seedlings have the lowest sur-
vival probabilities due to a high mortality caused by
seed predation and effects of direct solar radiation on
germinated seeds. These mortality factors determine
that survivorship curves of N. macrocephala seed-
lings are type III. This survivorship pattern also has
been reported for other species of cacti with very dif-
ferent life forms 共Godínez-Alvarez et al. in press兲.
The estimated growth rates indicate that popula-
tions of these species of Neobuxbaumia are in a nu-
merical equilibrium. Similarly, other species of
columnar cacti 共E. chiotilla, Ortega-Baes 2001; P.
pringlei, Silva 1996兲 present a population growth rate
that does not differ significantly from unity. On the
other hand, the estimated growth rate 共0.54兲 for C.
gigantea indicates that populations of this species are
declining 共Silvertown et al. 1993兲. These contradic-
tory results should be interpreted cautiously because
estimations of the population growth rates are based
in annual projection matrices which assume that tran-
sition probabilities are constant and populations grow
exponentially 共Caswell 1989兲. These assumptions
limit the use of matrix models to analyze the popula-
tion dynamics of columnar cacti since fluctuations in
the population numbers of these plants occur in de-
cades 共Pierson and Turner 1998兲.
With respect to reproduction, our results indicate
that fecundity values in N. macrocephala and N. te-
tetzo increase according to plant height. However, the
mean number of seeds per plant is lower in N. mac-
rocephala than in N. tetetzo. This low level of sexual
reproduction in N. macrocephala may decrease the
probability of establishment of new individuals,
affecting the size-frequency distribution of its popu-
lations. In fact, observing the actual size distribution
of this species, it is possible to argue that establish-
ment events occur less frequently than in N. tetetzo
population. Esparza-Olguín et al. 共2002兲 have indi-
cated that N. macrocephala reproduction is one aspect
of the life cycle that could limit the population
growth. The authors analyzing the demography of this
species with population projection matrices found
that a 10-fold increase in reproduction would result
in ␭ values larger than unity. Comparative studies of
closely-related species have suggested that abundance
and range distribution could be affected by different
aspects of sexual reproduction. Sparse species could
have low levels of sexual reproduction or show a
highly variable production of seeds among years
共Angevine 1983; Kruckeberg and Rabinowitz 1985;
Fiedler 1987; Byers and Meagher 1997兲. Other stud-
ies also have found that production of seeds and their
permanence in the soil seed bank may affect distribu-
tion and persistence of species 共Silva et al. 2000兲.
Pollen limitation of N. macrocephala flowers could
be one of the possible factors responsible for the low
number of seeds produced by this plant. The closely-
related sympatric species N. macrocephala, N. tetetzo,
and N. mezcalaensis flower simultaneously during the
year. Their flowers are self-incompatible having
similar anthesis periods and they are also pollinated
by the same species of nectar-feeding bat 共Leptonyc-
teris curasoae; Valiente-Banuet et al. 1996; Valiente-
Banuet et al. 1997兲. Moreover, these species have
striking differences in their population densities 共i.e.,
1680 ind/ha in N. mezcalaensis, 1200 ind/ha in N. te-
tetzo, and 200 ind/ha in N. macrocephala; Valiente-
Banuet and Ezcurra 1991, Valiente-Banuet et al.
1997, Esparza-Olguín et al. 2002兲. All this informa-
tion suggests that N. macrocephala flowers may have
a lower chance of being visited by L. curasoae than
those of N. tetetzo and N. mezcalaensis. When N.
macrocephala flowers are visited by bats, they could

receive pollen grains from congeneric species, prob-
ably inhibiting seed development.
Additionally, pre-dispersal seed predation may be
another factor that could also affect the sexual repro-
duction of N. macrocephala. Previous observations in
the field indicate that seeds of this species and those
of N. tetetzo are consumed by larvae of an unidenti-
fied moth. However, preliminary data show that seed
losses are apparently higher in N. macrocephala
共30%兲 than in N. tetetzo 共2%兲.
In conclusion, our results indicate that N. macro-
cephala and N. tetetzo have similar demographic pat-
terns. However, there are differences in their repro-
ductive traits. N. macrocephala has a lower level of
sexual reproduction than N. tetetzo which probably
decreases the probability of establishment of new in-
dividuals. Pollen limitation and pre-dispersal seed
predation could be some factors that limit N. macro-
cephala populations. Finally, it is important to bear
in mind that our results are based on the analysis of
just a single population of N. macrocephala, therefore
to completely understand the factors that constrain its
populations it is necessary to conduct studies repli-
cated for populations and years.
Acknowledgments
Leticia Ríos, Antonio Soriano, Rocío José, Carlos
Silva, Ariel Alcántara, Oscar Osorio, Adolfo Vital,
Luis Zepeda, and Olga García kindly assisted during
fieldwork. Arturo Flores and Leopoldo Valiente pro-
vided the statistical package GLIM release 4 and the
program written in the programming language Pascal.
Two anonymous reviewers provided constructive
comments that improve the manuscript.
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