Journal of Arid Environments (2002) 51: 89–102

doi:10.1006/jare.2001.0926, available online at http://www.idealibrary.com on

Evaluation of the conservation status of a rare cactus

(Mammillaria crucigera) through the analysis of its
population dynamics

Cinthya Contreras & Teresa Valverde*

Lab. Especializado de Ecologı´a, Facultad de Ciencias, Universidad Nacional

Auto´noma de Me´xico (UNAM), Circuito Exterior, Ciudad Universitaria,
Me´xico, D.F. 04510, Me´xico
We used population projection matrices to analyse the demography of
Mammillaria crucigera, a rare cactus endemic to a small region in Central
Mexico. Matrices were based on a 2-year period of observations on survival,
growth and reproduction. No seed germination or seedling survival were
observed; thus, these matrix entries were experimentally estimated. Popula-
tion growth rate (l) was lower than unity when low germination values (as
those expected in natural conditions) were applied. The highest elasticity
values corresponded to the survival of large adults. Matrix simulations
indicated that only significant increases in fecundity and seedling survival
resulted in positive l values.
# 2002 Elsevier Science Ltd.

Keywords: matrix models; cacti; Mammillaria crucigera; conservation; rare

species; demography; Tehuacan Valley; population dynamics

Introduction

The Cactaceae is a plant family distributed mainly in arid and semi-arid habitats of the
American Continent. At present, this group includes a particularly high number of
threatened species (Hunt, 1992; Anderson & Taylor, 1994). This is perhaps due to the
fact that cacti are highly vulnerable to disturbances, given their low individual and
population growth rates, high longevity, and low recruitment rates, which limit their
ability to recover after perturbation (Hernandez & Godinez, 1994; Hernandez &
Barcenas, 1995).
In recent years, many cacti populations have been subject to intense disturbances,
such as habitat fragmentation, illegal collection and trade, and land-use change
towards farming and cattle ranching (Arias, 1993). Thus, many cacti are facing
marked population declines that need urgent attention from conservation agencies
world-wide (Steenbergh & Lowe, 1969; Nobel, 1986; Zavala-Hurtado & Dı́az-Solis,
1995). This has led many biologists to include apparently endangered cacti species
into the several categories recognized by the IUCN or CITES. However, the inclusion
of these taxa in the lists of endangered species has often been based on isolated
observations, rather than on actual empirical data. Our knowledge of the population

*Corresponding author. Fax: 00-52-56-22-48-28. E-mail: mtvv@hp.fciencias.unam.mx

0140-1963/02/010089 + 14 $35.00/0 # 2002 Elsevier Science Ltd.

90 C. CONTRERAS & T. VALVERDE

behaviour of most of the species included in red lists is rather limited. The lack of
population studies on cacti is a matter of concern not only because of its implications
for conservation, but also because of the gap it creates in our understanding of
demographic patterns and life histories in plants.
In this study, we address the population dynamics of Mammillaria crucigera Martius,
a globular cactus endemic to a small region in the area of Tehuacan–Cuicatlan, in
Central Mexico. This species has been classified as vulnerable by IUCN and as rare by
CITES and the Mexican environmental agency (Hunt, 1992; IUCN, 1994; Norma
Oficial Mexicana, 1994), especially on the grounds of its limited distribution and high
habitat specificity. However, the demographic traits of this species and whether its
current population dynamics might result in a long-term population decline are
entirely unknown.
Demographic analyses are useful tools in the evaluation of the conservation status of
plant species, since they provide us with basic information about the growth, survival
and reproduction of individuals in different size/age classes within a population. These
parameters determine the long-term numerical behaviour of the population; their
evaluation within a given period of time allows us to project the long-term
consequences of current population trends (van Groenendael et al., 1988; Caswell,
1989). Matrix projection models have been widely used in this context. The advantage
of these types of models is that, in addition to long-term population growth rate (l),
they may also evaluate the importance of different life cycle transitions to population
dynamics. In particular, elasticity analyses reveal the most vulnerable stages of the
species’ life cycle, thus allowing us to hypothesize about the potential fate of a
population subject to different management practices (Esparza et al., 2002).
In this paper we analyse the demography of M. crucigera with the aid of Lefkovitch
matrices, incorporating empirical data on growth, reproduction and survival of
juveniles and adults obtained during a 2-year period, and observations on the species’
reproductive biology, from flower production to seed germination and seedling
establishment. We then use the matrices to carry out numerical simulations aimed to
throw light on the demographic conditions under which a positive population growth
rate would be attained. This information, along with our present knowledge on the
species limited distribution and habitat specificity, is offered as a basis to support the
allocation of a specific conservation category to M. crucigera.

Material and methods

The study site

This study was conducted in the municipality of San José Tilapa in the Mexican State
of Puebla, near the border of Oaxaca (181330 1200 N; 981360 4200 W), at a site locally
known as Cerro Blanco (‘white hill’). This site is located within a local basin of the
Tehuacan–Cuicatlan region, in Central Mexico, at an altitude of 1220 ma.s.l.
The area has a warm, sub-humid climate with a mean annual temperature of 221C
and a total annual rainfall of 408 mm, most of which falls during the summer months,
between June and September. Most of this area is covered by a dry tropical forest
(with species such as Bursera sp., Fouqueria sp., Cercidium sp., Acacia sp., and
Pachycereus weberii) on soils of mixed origin among which various rocky mounds, or
cliffs, rise several tens of meters high, forming large enclaves in which xerophitic
vegetation dominates (with species such as Ferocactus recurvus, Agave macroacantha,
Coryphanta sp., Cephalocereus columna-trajanii, Mammillaria sp., Opuntia pillosa).
These cliffs are formed mainly by limestone and silicates, and are the only
environment in which Mammillaria crucigera lives, reaching densities of 1 to 5
plants m2. A large portion of the dry tropical forest surrounding these cliffs has been
 EVALUATION OF THE CONSERVATION STATUS OF A RARE CACTUS 91

turned into farmlands; other portions are under a lot of pressure from goat raising and
cattle ranching. Goats may even climb the cliffs in search of food and may cause
disturbances of varying intensity.

The species

Mammillaria crucigera is a small globular cactus with a green-greyish coloration and

with one to several cylindric stems. Most large plants have several stems, produced by
dichotomic branching. Each stem shows well-defined tubercles forming spiral series;
tubercles bear a circular areole in the apex with 18–25 short radial spines and 2–4
central spines. The flowers, which are 7–13 mm long, emerge from among the
tubercles, from woolly axils, forming a crown near the tip of the stem. They are
generally reddish to purplish. Fruits may be either ‘external’ or ‘internal’. The so-
called ‘external’ fruits are clavate, 8–10 mm long and with a reddish colouration.
‘Internal’ fruits remain hidden among the tubercles once they are ripe; they are round,
whitish and contain, on average, the same number of seeds as ‘external’ fruits (ca. 20).
Mammillaria crucigera is endemic from Mexico (Bravo-Hollis & Sanchez-Mejorada,
1991); it is known to grow only from five locations (Martorell & Peters, pers. comm.),
all of which are distributed around and very close to the San José Tilapa site. Within
this area, M. crucigera establishes itself mainly on the vertical walls of limestone and
silicate cliffs. Based on its restricted distribution range and low population densities,
this species has been classified as rare (Hunt, 1992; Norma Oficial Mexicana, 1994)
and as vulnerable (IUCN, 1994).

Field methods

The study was carried out from the summer of 1997 to the summer of 1999 in Cerro
Blanco, one of the cliffs in which this species is found. Here we marked 230 juvenile
and adult plants of M. crucigera on the east-facing wall of the cliff. Plants were located
within 1 m2 permanent quadrats marked on the wall with paint. Each plant could be
individually located within its quadrat by x and y co-ordinate. Quadrats could be
reached through paths formed by wind erosion which ran parallel to the side of the
cliff. Occasionally, a ladder was used to reach some of the quadrats that were placed
on the high parts of the wall.
For each plant, we recorded the number of stems, and measured the diameter of
each stem with the aid of a calliper to calculate stem area. Total plant size was
estimated as the sum of the areas of all the stems in a plant. Plants were measured in
summer 1997–99, during the same dates each year. Measurements were taken during
the summer rainy season to make sure that stems were turgid and that diameter
increases from one year to the next were due to plant growth. Measurements of plant
growth, as well as observations on survival, allowed us to calculate transition
probabilities among size categories that were later incorporated in a Lefkovitch matrix.
To estimate the matrix fecundity elements, we carried out observations on the
reproductive phenology (flower and fruit production) and seed germination of
M. crucigera. Reproductive phenology was described through monthly records of
flower/fruit production during 20 months in the plants located within the permanent
quadrats. Additionally, 15 adult plants were followed outside the quadrats; these
plants were covered with a plastic mesh once they had finished flowering. Fruit
production was also recorded monthly in these plants, which were taken as controls to
be compared with the plants in the quadrats (uncovered). This allowed us to test
whether the apparent fruit production from plants in the quadrats was being
underestimated due to the activity of frugivores (mainly lizards).
92 C. CONTRERAS & T. VALVERDE

Fruits were collected to estimate the mean number of seeds per fruit and to perform
germination experiments. Some of these experiments were done under controlled
conditions (growth chambers and greenhouse conditions, on agar, local soil and pot
soilFsee Results for details); others were performed in the field to obtain actual
estimates of seed germination under natural conditions. In these experiments, we
scattered 70 2-month old seeds within each of 10 open mesh boxes half buried in the
soil. These boxes were designed to prevent seeds from being displaced and for
relocation purposes. Five of these boxes were located in shaded micro-sites, while the
other five were set in open micro-sites. All these micro-sites were chosen along one of
the paths that ran parallel to the side of the rocky mound, thus, they were mostly on
horizontal terrain rather than directly on the vertical walls of the mound. Seeds were
planted in the field during the summer of 1998. Seed germination was recorded
during the first 3 days after planting and then monthly for a year.
To estimate the probability of seedling survival in the field we planted seedlings and
followed them through time. Seedlings were obtained from the seed germination
experiments performed under controlled conditions. They were transplanted to small
pots and were kept in the greenhouse (in Mexico City) for 5 months. During this
period they were slowly acclimatized to the harsh conditions they experienced in the
field by slowly reducing the watering frequency and increasing the light intensity.
Seedlings were introduced to the field in summer 1998; they were planted evenly
spaced in 20  20 cm2 quadrats marked on the ground. Twenty-five seedlings were
planted in each of eight quadrats; four of these were located under the shade while the
other four were in open micro-sites. Seedling survival was followed daily until all seeds
died, shortly after planting.

Matrix analysis

The population dynamics of M. crucigera was evaluated through the construction of

two population projection matrices: for 1997–98 and 1998–99. Lefkovitch matrices
were used, in which plants are classified in size categories. In this case, we subdivided
the population in eight size categories, defined according to total plant size (i.e. the
sum of the areas of all the stems in a plant) (Table 1). We made sure that the number
of individuals in each initial category was large enough so as to allow us to estimate
robust transition probabilities. The seed category was not considered since it was
assumed (as is the case with other Mammillaria speciesFRojas-Arechiga, 1997;
Ruedas et al., 2000) that seeds do not remain viable in the soil for long periods of time;
they either germinate or die within the same season.

Table 1. Size categories used to classify the M. crucigera individuals within the
population studied
Category Area (cm2) Stage Reproductive
features
0 0–0?100 Seedlings Non-reproductive
1 0?101–1?075 Juveniles Non-reproductive
2 1?076–3?075 Adults Reproductive
3 3?076–10?075 Adults Reproductive
4 10?076–17?075 Adults Reproductive
5 17?076–24?075 Adults Reproductive
6 24?076–31?075 Adults Reproductive
7 431?076 Adults Reproductive
 EVALUATION OF THE CONSERVATION STATUS OF A RARE CACTUS 93

The transition probability of juvenile and adult plants to different size classes from 1
year to the next were calculated as the frequency with which plants in each category
experienced different fates, including death. The probability that seedlings grew to the
next size category (i.e. transition 0-1) was originally calculated from the results of
the seedling survival experiment detailed in the previous section; however, as no
seedling survival was observed (see Results below), an arbitrary low value was
incorporated in the matrix (0?001) assuming that only one out of a thousand seedlings
makes it to the next size category. Although the lack of detailed information on this
important life cycle stage is a drawback of our data set, the use of different
hypothetical values allowed us to evaluate the demographic conditions that would
render a growing population, as will be seen below.
The fecundity entries, located in the first row of the matrix, represent the average
contribution of the individuals in each size category to the first category. Thus, these
entries are given in ‘seedling’ units, and are a composite of both seed production and
seed germination probability. Seed production was evaluated from the reproductive
phenology observations carried out monthly for 20 months, from which fruit
production was assessed; the mean number of seeds per fruit was 20?0712?6
(mean7standard error; n ¼ 112). Seed germination probability was originally
calculated from the results of the field experiments. Again, since no results were
obtained in this section, we had to introduce an estimate (0?01) reflecting a low
germination probability. As in the case of the seedling establishment phase, the use of
different fecundity values in numerical simulations was an opportunity to analyse the
conditions under which the population would be self-maintaining.
We obtained population growth rate (l), the stable size-class distribution (W ) and
the size-specific reproductive value (V) by multiplying the projection matrix by a
vector representing population structure in terms of the number of individuals in each
size category at the beginning of the study. This procedure was repeated with each
resulting vector until its proportions remained constant, at which point the population
grows at a rate ¼ l. From the vectors V and W we calculated the sensitivity matrix (sij)
and the elasticity matrix. The elasticity matrix is composed of eij entries, which are
calculated as follows:




eij ¼ aij =l l=aij ¼ aij =l sij
Elasticity is a measure of the proportional sensitivity of l to proportional changes in
the aij. Since the sum of all the eij in an elasticity matrix equals unity, each eij may be
interpreted as the relative contribution of each matrix entry to l (de Kroon et al.,
1986; Caswell, 1989). The confidence intervals for l were calculated according to the
analytical method proposed by Caswell (1989):
X
2

V ð lÞ ¼ l=aij V aij
i; j

As transition probabilities show a binomial distribution, their variance was calculated

as



 
V aij ¼ aij 1  aij =n
The variance of fecundity entries was calculated using the information on the natural
variability in this parameter obtained directly from the field data. The standard error
(s) was calculated as the square root of the variance of l. Approximately 95%
confidence intervals were calculated as l72s.

Numerical simulations

In order to simulate particular management or conservation practices, we modified

the relevant entries in the population projection matrix by a certain amount and
94 C. CONTRERAS & T. VALVERDE

directly evaluated their effect on l. The entries that were modified were fecundity,
seedling establishment and survival. One of the reasons for choosing these particular
entries for the numerical simulations was that for two of them (i.e. seed
germinationFa component of fecundityFand seedling survival) we had only
estimates instead of direct field observations.

Results
Early phases of plant development

Since no germinating seeds or young seedlings were observed in the field, we

tried to estimate the value of the matrix entries concerning seed germination and
seedling establishment through field experiments. In the germination experiments
(700 seeds sown, 350 under the shade and 350 in open conditions), we did not
observe a single germinating seed after 1 year. However, these results must be taken
cautiously as the seeds were followed monthly and we could have missed germination
events between observation dates, especially during the first month after sowing which
coincided with the rainy season. Since no field data were available for the seed
germination phase of the life cycle, an estimate (i.e. 0?01 ¼ 1%) had to be
incorporated in the calculation of the fecundity values in order to build population
projection matrices.
The results of seeds germination under controlled conditions show that seed
viability oscillated, on average, around 60%, with values between 8?5% and 82?3%,
depending on seed age and substrate conditions (Table 2). The highest germination
percentage was obtained on soil from the study site, rather than on agar. Seeds started
germinating 12 days after sowing and the maximum germination percentage was
achieved on day 23. The seedlings obtained in these germination experiments were
introduced to the field as part of the seedling establishment experiments. A total of
200 seedlings was introduced in June 1998. One day after their introduction we
observed no surviving seedlings. Therefore, the relevant matrix entry had to be
estimated. We gave it a value of 0?001, assuming that one seedling out of 1000 is
established; this assumption appears more or less reasonable, compared to other
Mammillaria species (López-Villavicencio, 2000) and considering the high aridity of
the habitat these plants occupy.

Reproductive phenology

The flowering period of M. crucigera in the study site started in November and ended
in May, with maximum flower production in February. Fruits (both ‘internal’ and
‘external’) were produced all year long, but maximum fruit production occurred in
April–June (Fig. 1). The reason as to why fruits were produced long after the last
flowers were observed appears to be the long time required for fruits to ripen. Flower
production was similar in 1998 and 1999; however, fruits were more abundant in
1998 than in 1999. The comparison of fruit production between the plants covered
with a plastic mesh after flowering and those within the quadrats (uncovered) showed
that fruit production was almost identical in both groups (results not shown), which
suggests that our data on fruit production were not significantly affected by frugivore
activity.
Plant fecundities were calculated from our observations on fruit and seed
production per plant, as well as on the estimate of seed germination probability.
Therefore, fecundity is given here as the contribution of adult plants to the seedling
stage. Plants of size category 1 contribute less than one seedling per plant to
the next generation, and this contribution increases with plant size (Table 3). In
 EVALUATION OF THE CONSERVATION STATUS OF A RARE CACTUS
Table 2. Germination percentage of M. crucigera seeds under controlled conditions. The number of seeds per replicate varied from 25 seeds (in
test No. 1) to 200 seeds (in test No. 3)
Tests No. of Sowing date Substrate Seed age % germination Day of first
replicates (months) germination
1 5 November 1997 Agar 2% 1 8?5 nr
2 1 February 1998 Pot soil 1–2 77?19 nr
1 Soil from the study site 82?35 nr
3 August 1998 Soil from the study site
1 10 67?61 12
1 3 41?00 12
1 2 76?44 12
nr ¼ not registered.

95
96 C. CONTRERAS & T. VALVERDE

3
Average number of reproductive
structures per plant 2.5

1.5

0.5

0
Dec (97)
Jan(98)

Jan(99)
Nov

Sep

Dec
Nov

Feb
Feb

May

May
Jun
Jun
Jul
Mar
Apr

Aug

Mar
Oct

Apr
Time (months)
Figure 1. Reproductive phenology of the M. crucigera population studied from November
1997 to June 1999: flower buds ( ); flowers ( ); fruits ( ).

Table 3. Size-specific fecundities for the M. crucigera population during (a)

1997–98 and (b) 1998–99. The mean number of seeds per fruit used to obtain the
data in the fifth column was 20? The germination probability used to obtain the
sixth column was 0?01
Size category n No. of fruits/ Mean no. of Mean no. of Seedlings/
category fruits/plant seeds/plant plant
(a)
0 1000 0 0 0 0
1 23 30 1?304 26?087 0?261
2 33 213 6?455 129?091 1?291
3 48 298 6?208 124?167 1?242
4 33 290 8?788 175?758 1?758
5 22 165 7?500 150?000 1?500
6 18 237 13?167 263?333 2?633
7 40 638 15?950 319?000 3?190
(b)
0 1000 0 0?000 0?000 0?000
1 11 0 0?000 0?000 0?000
2 24 0 0?000 0?000 0?000
3 43 15 0?349 6?977 0?070
4 32 27 0?844 16?875 0?169
5 20 24 1?200 24?000 0?240
6 19 28 1?474 29?474 0?295
7 57 262 4?596 91?930 0?919

1998/99 fecundities were lower than in the previous year, mainly due to a reduced
fruit production. In 1998/99, none of the categories had a fecundity value above one
(Table 3).
 EVALUATION OF THE CONSERVATION STATUS OF A RARE CACTUS 97

Matrix results

Population growth rate (l) was below unity for both the 1997–98 and the 1998–99
periods (Table 4). In 1997–98, l did not differ significantly from unity, but the results
of the 1998–99 matrix suggest a declining population, with a l value clearly below
unity. The difference in l between the 2 years was given mainly by lower fecundities,
and higher mortalities and retrogressions in 1998–99, compared to the previous year.
In 1998–99, individuals reproduced only from category 3 onwards and none of the
reproductive categories reached a fecundity value above unity (Table 4). Fecundities
are low in both matrices, which were determined by the low germination probability
incorporated in the calculation of this parameter. In general, individuals in larger size
categories showed higher fecundities. Mortality tended to decrease towards larger size
categories; none of the plants in category 6 died during the study period.
The population projection matrices obtained show that the entries with highest
values were those referring to the persistence of individuals in their same category,
followed by growth, which most frequently occurred in the next size category and
sometimes included leaps of four or five size categories. Also, the number of plants
decreased in size; thus, the matrices include retrogressions of as much as three size
categories. These retrogressions mainly were a result of the loss of stems due to
predation, rotting, loss of vigour or detachment from the substrate.
The stable size-class distribution (vector W ) for both matrices shows a high
proportion of individuals in the first category, followed by the last one. According to
the matrix from 1997–98, the expected size-class distribution at equilibrium would
include over 75% of the population in the seedling category, whereas according to the
1998–99 conditions, the population would be composed of 48% seedlings and 47%
large adults, while the rest of the categories would be represented by less than 5% of
the population (Table 4). The reproductive value increases with increasing plant size
and for the smallest individuals it was zero. This is due to the fact that there was no
reproduction in this size class and the probability of growing to reproductive size
classes was very low.
Elasticity analysis

For both matrices, the highest elasticity value corresponded to the survival and
persistence of the largest individuals (Table 5). This entry alone accounted for 97% and
95% (for 1997–98 and 1998–99, respectively) of the value of l. The elasticity for
fecundity entries was virtually zero, and for the entries referring to growth it was between
1% and 2% of the value of l. This elasticity pattern shows that in a declining population
(lo1) the value of l is mainly determined by the rate at which adult plants die.

Numerical simulations

The numerical simulations were performed only with the 1997–98 matrix in order to
test the potential effect of different demographic scenarios. We found that when the
fecundity entries were decreased from their original value to a value 15 times lower, l
changed only from 0?977 to 0?975. However, when the fecundity entries were
increased, the resulting change in l was more noticeable, reaching a positive value (i.e.
l41) when fecundities were 15 times higher than the original values. Additionally, a
ten-fold increase in seedling recruitment probability did not result in a l value above
unity, and significant decreases in this matrix entry resulted in only slight changes in l.
Changes in mortality entries, whether increasing or decreasing them up to 20% of
their original values, did not result in noticeable changes in l. Finally, when both
fecundity and seedling establishment probability were modified simultaneously, a
four-fold increase was enough to a render a positive population growth rate.
 98
Table 4. Population transition matrices for the M. crucigera population for the periods (a) 1997–98 and (b) 1998–99
0 1 2 3 4 5 6 7 W V
(a) l ¼ 0?97770?049
0 0 0?261 1?291 1?242 1?758 1?500 2?788 3?190 0?763 0?000
1 0?001 0?425 0?030 0 0 0 0 0 0?001 0?109
2 0 0?391 0?455 0 0 0 0 0 0?001 0?121
3 0 0?087 0?424 0?563 0 0 0 0 0?001 0?141

C. CONTRERAS & T. VALVERDE

4 0 0 0 0?33 0?485 0 0 0 0?001 0?155
5 0 0 0 0?042 0?242 0?455 0 0 0?001 0?154
6 0 0 0 0 0?152 0?364 0?333 0 0?001 0?163
7 0 0 0 0 0?091 0?136 0?667 0?975 0?231 0?157
Qx 0?999 0?087 0?090 0?063 0?030 0?045 0 0?025
n 100 23 33 48 33 22 18 40
(b) l ¼ 0?89670?077
0 0 0 0 0?070 0?169 0?240 0?295 0?919 0?483 0
1 0?001 0?545 0?083 0?023 0 0 0 0 0?005 0?072
2 0 0?273 0?417 0?093 0 0?050 0 0 0?008 0?095
3 0 0 0?208 0?465 0?188 0?050 0?158 0 0?014 0?102
4 0 0 0 0?140 0?500 0?150 0?053 0 0?011 0?116
5 0 0 0 0?070 0?156 0?250 0?158 0 0?006 0?175
6 0 0 0?042 0 0 0?300 0?368 0 0?005 0?209
7 0 0 0?042 0?023 0 0?100 0?263 0?895 0?467 0?232
Qx 0?999 0?182 0?208 0?186 0?156 0?100 0?000 0?105
n 100 11 24 43 32 20 19 57
The l values (along with their 95% confidence intervals) are given above each matrix. Qx ¼ mortality rate; n ¼ number of individuals from which transitions in each
column were calculated. Numbers in the main diagonal are underlined to facilitate reading.
 EVALUATION OF THE CONSERVATION STATUS OF A RARE CACTUS 99

Table 5. Elasticity matrices for the M. crucigera population studied, correspond-

ing to (a) 1997–98 and (b) 1998–99
0 1 2 3 4 5 6 7
(a)
0 0 1?1E06 4?3E06 5?4E06 5?2E06 2?6E06 4?9E06 2?2E03
1 0?002 0?002 0 0 0 0 0 0
2 0 0?002 0?002 0 0 0 0 0
3 0 0 0?002 0?003 0 0 0 0
4 0 0 0 0?002 0?002 0 0 0
5 0 0 0 0 0?001 0?001 0 0
6 0 0 0 0 0?001 0?001 0?001 0
7 0 0 0 0 0 0 0?002 0?973
(b)
0 0 0 0 7?9E07 1?4E06 1?2E06 1?2E06 3?3E04
1 0 0?002 0 0 0 0 0 0
2 0 0?001 0?003 0?001 0 0 0 0
3 0 0 0?002 0?007 0?002 0 0?001 0
4 0 0 0 0?002 0?006 0?001 0 0
5 0 0 0 0?002 0?003 0?003 0?001 0
6 0 0 0?001 0 0 0?004 0?004 0
7 0 0 0?001 0?001 0 0?001 0?003 0?946

Discussion

Our demographic analysis was based on empirical observations of survival,

reproduction and growth of M. crucigera plants in natural conditions. However, we
lacked sufficient empirical information on seed germination and seedling establish-
ment; thus, the matrix entries related to these life cycle stages had to be estimated by
giving them arbitrarily low values, reflecting in some way the results of our field
experiments. Yet, the fact that no seeds germinated and no seedlings survived as part
of our field experiments cannot be interpreted, though, as a total experimental failure;
these results reflect clearly that these life cycle stages represent a dramatic bottleneck
in the population dynamics of this species and are responsible to a large extent for the
low population growth rates observed.
Although no seed germination was observed in natural conditions, we had high
germination percentages under controlled conditions. Note that the highest
germination percentages were obtained when using soil from the study site as
substrate. This preference for this particular type of substrate during such early
developmental stages may account to some degree for the high habitat specificity of
M. crucigera. Additionally, the germination response of M. crucigera seeds under
controlled conditions was slower compared to other cacti species. For instance,
Mammillaria magnimamma, Astrophytum miryostigma and Carnegia gigantea seeds start
germinating 3, 4 and 5 days after sowing, respectively (Steenbergh & Lowe, 1969;
Berinstain, 1997; Ruedas et al., 2000), while M. crucigera started germinating on day
12. This feature suggests that M. crucigera seeds would germinate under natural
conditions only in years when the rain pattern allows the continued presence of soil
humidity for a certain number of days.
M. crucigera starts flowering in early winter, as is the case for other Mammillaria
species found near the study area (M. pectinifera, M. napina, M. hernandeziiF
100 C. CONTRERAS & T. VALVERDE

E. Peters, C. Martorell and S. Arizaga, pers. comm.). In contrast with what was
observed for certain columnar cacti which reproduce almost synchronically (Steen-
bergh & Lowe, 1969; Godinez-Alvarez et al., 1999; Esparza et al., 2002), globular cacti
tend to show longer reproductive periods and in the case of M. crucigera, plants flower
for 5 months and fruit almost all year long. Other authors have suggested that these
long reproductive periods may result in a reduced intra-specific competition for
pollinators and seed dispersers (del Castillo, 1982; Leon & Valiente-Banuet, 1994).
Variation in plant fecundity and mortality was the main factor that determined the
observed variations in population growth rate. The l value for 1997–98
(0?97770?049) did not differ significantly from unity; however, in 1998–99 we
obtained a lower l (0?89670?077), suggesting a declining population. In 1998–99,
the mortality rate of individuals in size categories 1–5 and 7 was more than twice that
of 1997–98, and the fecundity values were in some cases one order of magnitude
higher in 1997–98 than in the following year. This variability in the demographic
behaviour through time could give rise to long-term variation in population numbers,
which appears to be a common feature among plants from semi-arid regions.
In addition to inter-annual variation, fecundity also varied between categories,
showing higher values as plant size increased. This pattern has also been reported for
other cacti both columnar and globular, such as Carnegia gigantea, Neobuxbaumia
tetetzo, N. macrocephala, Lophocereus schottii, Coryphanta robbinsorum and M.magni-
mamma (Steenbergh & Lowe, 1977; Parker, 1987, 1989; Schmalzel et al., 1995;
Godı́nez-Alvarez et al., 1999; Esparza et al., 2001), and may result from the branching
of larger plants which gives rise to a higher number of potential flowering buds. On the
other hand, mortality showed the inverse pattern, with smaller plants having a much
higher mortality probability than larger plants. An important death cause was parasite
herbivore attack. Plants with only one stem (i.e. smaller plants) had lower survival
probabilities after herbivore attack, while larger plants could often recover from it.
Another death cause which affected both small and large plants was erosion; this
resulted in the uprooting of plants established on the cliff walls, most of which died a
few months later.
Observed population structure, in terms of the number of individuals in each size
category, was different from the stable size-category distribution projected by the
matrix iterations. Plants in category 7 were the most abundant and plants in categories
2–4 were also well represented, while seedlings were practically absent (Table 4). This
suggests that seedling germination and seedling establishment may be even lower than
what we estimated. Thus, although one of our matrices (1997–98) suggests a
population near the numerical equilibrium with l not significantly different from
unity, it is clear that mortality exceeds new recruitments which in the long run would
result in a rapidly declining population. In fact, we have estimated that the smallest
individuals recorded in our sample were around 8 years old (Contreras 2000); this
would mean that no seedling establishment has occurred in quite a long time.
The germination and early growth stages are of paramount importance for the
maintenance of the population. Our matrix simulation results showed that only
increases in seedling survival and seed germination rendered positive population
growth rates. Thus, any management plan aimed at the preservation of this species
should consider the direct manipulation of these life cycle stages in order to increase
the survival probabilities of these phases.
The demographic features of the M. crucigera population studied suggest that its
ability for population growth is severely limited. Additionally, its high habitat
specificity and small distribution range are features that make this species vulnerable
to local management practices which include cattle ranching, habitat fragmentation
and land-use change towards altered ecosystems. If current land management
tendencies were to continue, M. crucigera populations could eventually be under
serious threat. This has led us to propose the change in the status of M. crucigera, from
 EVALUATION OF THE CONSERVATION STATUS OF A RARE CACTUS 101

rare to vulnerable in the Mexican environmental agency (Norma Oficial Mexicana,

1994), which coincides with the category given to this species by the IUCN (Hunt,
1992; IUCN, 1994).
It is important to carry out research to analyse the physiological requirements and
constraints of M. crucigera during the early stages of development in order to
eventually design reintroduction programmes. Also, it would be important to study in
more detail the distribution and abundance patterns within this and other potentially
colonizable areas, as well as genetic aspects of existing populations which, along with
our demographic data, would offer some insight into the persistence probability (i.e.
viability) of populations.

We are grateful to Elena Vilchis, Ligia Esparza, Marcela Ruedas, Ariel Arias, Sandra Quijas and
José Miguel Pickering for assistance in the field. We also thank Mariana Hernández Apolinar,
Pedro Eloy Mendoza and Marco Antonio Romero for technical support, both in the field and
with data management. Part of this project was carried out with the financial support of
CONABIO (Project No. R-129); additionally, the first author received a one-year studentship
from Fundación UNAM.

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