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Plant Ecol (2010) 210:5366

DOI 10.1007/s11258-010-9737-6

Demography of an endangered endemic rupicolous cactus


Alejandro Flores Martnez Gladys Isabel Manzanero Medina
Jordan Golubov Carlos Montana Mara C. Mandujano

Received: 2 September 2009 / Accepted: 12 February 2010 / Published online: 27 February 2010
 Springer Science+Business Media B.V. 2010

Abstract We compared the demography of two


populations of Mammillaria huitzilopochtli, an endemic and threatened rupicolous cacti species with a
narrow distribution in the semiarid Tehuacan-Cuicatlan region of central Mexico. Censuses were
conducted over a 5-year period in two populations:
A. F. Martnez  G. I. M. Medina
Centro Interdisciplinario de Investigacion para el
Desarrollo Integral Regional, Unidad Oaxaca, Instituto
Politecnico Nacional (CIIDIR IPN Oaxaca), Hornos 1003,
C.P. 71230 Santa Cruz Xoxocotlan, Oaxaca, Mexico
e-mail: alexfmtz62@gmail.com
G. I. M. Medina
e-mail: gmanzane@ipn.mx
J. Golubov
Lab. Ecologa, Sistematica y Fisiologa Vegetal, Depto. El
Hombre y Su Ambiente, Universidad Autonoma
Metropolitana Xochimilco (UAM Xochimilco),
Calzada del Hueso 1100, Col. Villa Quietud,
04960 Coyoacan, DF, Mexico
e-mail: gfjordan@correo.xoc.uam.mx
C. Montana
Instituto de Ecologa, A. C., Carretera Antigua a Coatepec
Km 2.5, Apartado Postal 63, C.P. 91000 Xalapa,
Veracruz, Mexico
e-mail: carlos.montana@inecol.edu.mx
M. C. Mandujano (&)
Depto. Ecologa de la Biodiversidad, Instituto de
Ecologa, Universidad Nacional Autonoma de Mexico
(UNAM), Apdo Postal 70-275, 04510 Mexico, DF,
Mexico
e-mail: mcmandu@miranda.ecologia.unam.mx

a disturbed site (S1) and a well-preserved site (S2).


Five annual size-based matrices and a mean transition
matrix of each population were constructed to
estimate demographic trends. Prospective timeinvariant analyses were performed to calculate population growth rate and elasticities, whereas prospective stochastic analyses were performed to assess
quasi-extinction probabilities and how simulated
changes in recruitment, stasis and growth affected
the population growth rate. Retrospective perturbation analyses (life table response experiments,
LTREs) were used to explore the contributions of
demographic processes, plant sizes, and temporal
variability (years) to the observed variations in
population growth rate. The species showed decreasing population growth rates for almost all years and
sites, S1 showed lower population growth rates than
S2. Quasi-extinction probabilities were 1 after
9 years for S1 and 17 years for S2. Elasticity values
were highest for matrix entries corresponding to
plants remaining in the same category (stasis)
followed by growth and fecundity. LTREs showed
that fecundity had negative contributions to population growth rates for all years in S1 population, while
it had positive contributions in 4 out of 5 years in
population S2. Prospective stochastic analyses
showed that increasing recruitment by 50% could
give population growth rates [1 in S2 while none of
the simulations give this value in S1. Increasing
survival also raises population growth rates but
always below one. These results indicate that

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populations under the influence of human disturbance


will eventually be lost. According to the models the
most promising management strategy to conserve this
species is to increase recruitment rates and to give
special care to reproductive adults.
Keywords Cactaceae  Demography 
Elasticity  LTREs  Mammillaria huitzilopochtli 
Matrix model  Perturbation analysis

The Cactaceae family, endemic to the New World, is


made up of around 2000 species (Anderson 2001). In
the Americas, Mexico has one of the highest diversity
of cacti, both at the generic (63 genera) and specific
levels (&670 species; Bravo Hollis 1978; Guzman
et al. 2003). Species diversity comprises approximately 37% of total cacti species of which nearly
84% are endemic to Mexico (Arias et al. 2005).
Currently, this group includes a particularly high
number of threatened species (Anderson et al. 1994;
Arias et al. 2005). Their threatened status is mostly
due to the fact that cacti are vulnerable to disturbance, have high habitat specificity which limits their
ability to recover after natural or anthropogenic
disturbance, low individual and population growth
rates, high mortality during juvenile phases, and low
recruitment rates (Schmalzel et al. 1995; Contreras
and Valverde 2002; Esparza-Olgun et al. 2002;
lvarez et al. 2004; Mandujano et al. 2007b).
2005; A
In arid environments, extreme temperatures, unpredictable precipitation (Valiente-Banuet and Ezcurra
1991), and the pressure of herbivores (Cody 1993)
lead to new seedlings of succulents establishing only
rarely. Successful seedling establishment usually
occurs under the canopy of nurse plants or inanimate
objects, which both mitigate such harsh conditions
and protect seedlings from herbivores. However, the
relative importance of factors in controlling seedling
establishment varies among species (e.g. Mandujano
et al. 1998, 2002; Esparza-Olgun et al. 2002, 2005;
Navarro and Guitian 2003; Valverde et al. 2004;
Carrillo-Angeles et al. 2005; Valverde and ZavalaHurtado 2006, Mungua-Rosas and Sosa 2008).
The population structure and dynamics of perennial plants is the result of the demographic processes
of reproduction, establishment, growth, and survival
over many generations, but most population models
in cacti employ the simplifying assumption that the

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Plant Ecol (2010) 210:5366

environment is constant and analyze a single population for few time intervals (Valverde et al. 2004;
Valverde and Zavala-Hurtado 2006; Mandujano et al.
2007b). Most ecosystems, however, can be heterogeneous in both time and space showing strong
variation in their environmental conditions among
years (Mandujano et al. 2001, 2007a; Esparza-Olgun
et al. 2005). Recognizing the importance of this
heterogeneity on population behavior has resulted in
an increase in the number of studies that contrast the
population structure and dynamics between habitats
and time intervals (e.g. van Groenendael and Slim
1988; Svensson et al. 1993; Navarro and Guitian
2003; Esparza-Olgun et al. 2005; Mandujano et al.
2007a).
Traditionally, the population dynamics of plant
species have used transition matrix models (van
Groenendael and Slim 1988; Silvertown et al. 1993;
Svensson et al. 1993; Menges 2000; Caswell 2001,
Ramula 2008). These models constitute a powerful
analytical tool since they allow the projection of the
potential fate of a population under different theoretical scenarios, as well as the evaluation of the
relative contributions of the demographic processes
occurring in different life cycle stages (de Kroon
et al. 1986; Silvertown et al. 1993). The use of
stochastic matrix models, which allow the inclusion
of the spatial and temporal environmental variability
into the analysis of the long-term population dynamics (Caswell 2001; Mandujano et al. 2001; Pico and
Riba 2002; Valverde et al. 2004; Boyce et al. 2006),
has recently demonstrated that the effect of stochasticity on the long-term fate of populations may
depend on an interaction between life history traits
and sensitivity to environmental variance. In this
context, stochastic demographic analyses may contribute to our understanding of the causes of rarity, at
least in the aspect concerned with limitation in
population numbers and rates of seedling recruitment.
Many cacti populations have been subjected to
intense perturbations, such as habitat fragmentation,
illegal collection and trade, and land use change
toward farming and cattle ranching. Consequently,
several species are now facing marked population
declines that need urgent attention (Anderson et al.
1994; Carrillo-Angeles et al. 2005; Mandujano et al.
2007b). This need for information is in striking
contrast to the few number of species that have been
studied from a demographic point of view (Godnez-

Plant Ecol (2010) 210:5366

Alvarez et al. 1999, 2003; Esparza-Olgun et al. 2002,


2005; Valverde et al. 2004; Clark-Tapia et al. 2005;
Mandujano et al. 2001, 2007a, b; Valverde and
Zavala-Hurtado 2006; Jimenez-Sierra et al. 2007),
even though demographic information is needed for
adequate conservation measures (Schemske et al.
1994). In addition, most studies have been done over
short time periods contributing information of limited
value to understand the long-term trends of population parameters.
In this study we analyzed the population dynamics
of Mammillaria huitzilopochtli Hunt, a globose
cactus endemic to a small region of central Mexico,
listed as endangered under Mexican legislation on the
grounds of its limited distribution and illegal collection of specimens (Rabinowitz et al. 1986; GarcaMendoza et al. 1994; SEMARNAT 2002; Arias et al.
2005). Populations of this rupicolous species inhabit
cliffs in which gravity prevents soil accumulation,
and humidity is limited due to rapid runoff.
Over a 5-year period we studied two out of the
seven remaining populations. The two populations
differ in the degree of anthropogenic disturbance
(well-preserved and disturbed) in Oaxaca, Mexico.
We set up matrix population models, perturbation
analyses, and simulations (Caswell 2001) to address
three questions. (1) Are the populations declining?
(2) What are the most sensitive life history components for population growth through time (years) for
each population? and (3) When incorporating stochasticity, what are the potential long-term consequences of the observed short-term demographic
behavior for each population?

Materials and methods


Study species and sites
Mammillaria huitzilopochtli D. R. Hunt is a globose
at first and later cylindrical rupicolous cactus with a
single stem and dark green coloration. Flowering
occurs between September and November, and the
red colored flowers (1217 mm long) are arranged in
a crown near the tip of the stem. The clavate 15
25 mm long fruits mature from April to July, and
have reddish to brown red coloration once ripe
(Anderson 2001). The species is found in the
Oaxacan portion of the Tehuacan-Cuicatlan

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Biosphere Reserve, Mexico, a floristic region recognized as a center of endemism and diversity of cacti
and other species (Villasenor et al. 1990). The species
grows in xerophilous scrub and dry tropical forest,
and populations are fragmented into small local
populations that are relatively far from each other.
Only seven populations are known to actually exist
(Peters and Martorell 2000), and they are established
on a total surface of 1058 ha, with a density ranging
from 450 to 6300 ind/ha. This study was carried out
from 1999 to 2004 (5 years of demographic data) in
the Cuicatlan Valley (17480 N, 96580 W) where
mean annual rainfall is 553 mm, most of which falls
between June and September, and a mean annual is
temperature of 25.5C. In 1999 when we started this
study, three populations were reported to exist, one of
which (Distrito de Etla) when revisited had already
been destroyed by urban development. The two
remaining populations were the ones reported in
herbarium specimens at the time (Voucher specimens
in Mexico City, Mexico MEXU 474935, 518191,
790174, 202345, 387911). The two populations were
living under contrasting disturbance conditions (Flores-Martnez and Manzanero 2005). The first site
(disturbed site, hereafter S1, 17480 4100 N,
96570 5000 W) is in an area fragmented by housing,
road construction, and sand-mine operations. The
second site (conserved site, hereafter S2,
17540 1900 N, 96570 5600 W) is 18 km north of S1
and still has large portions of native vegetation cover.
The sites also differed in plant density (900 ind/ha in
S1 and 3850 ind/ha in S2). The species is very
patchily distributed in its distributional range; so
extrapolations of total number of individuals are
always overestimates. Both sites have Neobuxbaumia
tetetzo (F.A.C. Weber) Backeb. as the dominant
species with associates Escontria chiotilla (F.A.C.
Weber) Rose, Pachycereus weberi (J.M. Coulter)
Backeb., Myrtillocactus geometrizans (Mart.) Console, Hechtia sp., Turnera difusa Willd, Plumeria
rubra L., and Bursera morelensis Ramrez. Individuals of M. huitzilopochtli can be found on both sides
of gorges running through the area, with no relation
of the number of individuals or their density with the
cardinal orientation of the slope. Since the beginning
of our study, individuals found in the vicinity of our
permanent plot at S1 were killed by the construction
of a secondary road leading out of the town of
Cuicatlan. We found no differences in rainfall

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regimes (t = 2.117, df = 10, P [ 0.05) during the


study period or in soil characteristics between sites
(Flores-Martnez 2008). To characterize disturbance,
we used the method proposed by Martorell and Peters
(2005) that uses 14 different metrics that incorporate
human activities, livestock raising, and land degradation into a weighted relative disturbance index
(DI = 0.1334 GOAT - 0.1631 CATT ? 0.1334
BROW ? 0.0799 LTRA - 0.1257 COMP ? 0.1931
FUEL - 0.0231 LTRA ? 0.0758 TRAS ? 0.1389
PROX ? 0.1371 CORE ? 0.0929 LUSE ? 0.1133
EROS ? 0.1837 ISLA ? 0.1009 TOMS) that varies
from 0 to 100 (0 being less disturbed).
Population dynamics
Transition matrix construction
All individuals within each population (N = 197 in
S1 and N = 476 in S2) were labeled, mapped, and
surveyed annually in the month of July from 1999 to
2004 (5 years of demographic data), and fruits were
counted during summer. Each individual was measured (height) with the aid of a caliper to the nearest
0.01 mm as height more accurately described the
growth of the single shoot apical meristem than other
morphological measurements.
In order to examine population dynamics five
annual size-transition matrices were constructed for
each population studied (S1 and S2). Populations
were structured into five classes, which were a
combination of size (cm) and stage: seedlings C1,
juveniles C2 (0.12 cm), young adults C3 (2.1
4 cm), mature adults C4 (4.16 cm), and old adults
C5 ([6.1 cm) included the last size class that actually
changed shape due to gravity.
The seed category was not considered in matrix
construction because seeds rapidly lose viability in
periods greater than 1 year (Flores-Martnez et al.
2008). Entries for fecundity, located in the first row of
the matrix (elements a1j), represented the average
contribution of the individuals in each size category to
the seedling class. Since no establishment of seedlings
was found during the study period, fecundities (entries
a1j) were assessed by multiplying the number of fruits
per plant in each size category (from the yearly census)
times mean seed production (43 seeds per fruit) times
the mean proportion of seed germination (0.89)
divided by the number of individuals found in each

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size class. Seed germination was estimated through


laboratory experiments with seeds\1-year-old kept at
room temperature and germinated in humid filter paper
(Flores-Martnez et al. 2008). Owing to the difficulty
of estimating seed mortality and evidence of high fruit
consumption in the field, the value of fecundity was
multiplied by 0.1% to get final fecundities (a1j), a value
that reflects the rare establishment of individuals in the
Cactaceae and also makes the life cycle adequate for
analysis (Mandujano et al. 2001; Contreras and
Valverde 2002). In order to determine seedling
survival under field conditions, seedlings were germinated in controlled conditions, acclimatized by watering spaced into 2 week periods, and transplanted to
field conditions during September 2002 at each site. As
previous experiments showed no seedling survival
under direct solar radiation we used the two most
common nurse plants (see Flores-Martnez 2008).
Seedlings were followed for 8 months, and the values
of final survival (0.15 for S1 and 0.125 for S2) were
used for analysis (entry a21).
For each habitat we constructed two kinds of
transition matrices: (1) annual matrices, based on the
data for each year, and (2) mean matrices, constructed by averaging the class-specific individual
number values for the five matrices at each site. The
matrix population model was: nt ? 1 = A nt, where
A is the transition matrix and nt is a vector which
includes the numbers of individuals in the stage
classes in time t (Caswell 2001). The program
MATLAB-PC ver 7.0 (The MathWorks Inc, MA,
USA) was used for all matrix analyses. Confidence
intervals for the finite rate of population growth (k)
were estimated using the series approximations
P P
proposed by Caswell (2001): V(k) = i,j
kl
Cov(aij, ajk)(qk/q aij)(qk/q akl). Because transition
probabilities represent estimates of the binomial
parameter, p, the variance was calculated as
V(aij) = aij (1 - aij)/n the SE of k was then the
square root of V(k), and 95% confidence intervals
were k 2SE(k) (Caswell 2001). Annual projection
matrices were used to characterize the population
dynamics, determine changes in k between years and
sites, and assess changes in mortality rates and
reproductive values between years (Mandujano et al.
2001). Mean matrices were also used to determine
differences in population growth rates, compare vital
rates between sites, and to represent the life cycle
diagram.

Plant Ecol (2010) 210:5366

The contribution of the vital rates toward population growth was assessed through the construction of
sensitivity and elasticity matrices, a prospective
approach that helped us determine how k would be
affected by changes in survivorship, growth, and
fecundity (de Kroon et al. 1986; Mandujano et al.
2001; Boyce et al. 2006).
Life table response experiments (LTREs)
Life table response experiments (LTREs, Horvitz
et al. 1997; Caswell 2001) were used to estimate the
contribution of year, plant size, and site to the
variation of k in one analysis, and of year, site, and
demographic process to the variation of k the
elasticities of k in a second analysis. These analyses
provided a means of exploring the contribution of any
given entry from the transition matrix to the observed
value of k (Horvitz et al. 1997; Tickin and Nantel
2004; Mandujano et al. 2007a). LTREs have n
treatments (in this case n = 10, two levels of site
and five levels of year), yielding population projection matrices A(m) and rates of increase k(m) for
m = 1,,n. The main effects of each factor and the
interactions among factors in two-way cross-classified treatments can be decomposed. A(m) = A(ij) was
the transition matrix resulting from the ith level of
time (years, with five levels, 20002001, 20012002,
20022003, 20032004, and 20042005) and the jth
level of site (S1 or S2), and k(ij) its eigenvalue. A(r)
was the reference population projection matrix (mean
matrix, overall S1 and S2 by year combinations) with
corresponding rate of increase k(r). The effect of a
treatment m on k was then decomposed into contributions from each of the matrix entries (Caswell
2001).
Numerical simulations
We used numerical simulations to find out how
changes in demographic parameters would impact
population growth rates. In these models the population growth rate depends on different conditions
(annual matrices that have a certain probability of
occurrence), in such a way that a temporal sequence
of annual projection matrices is generated by a
stochastic process (Caswell 2001). To estimate ks (the

57

stochastic growth rate) we used the popbio package


(Stubben and Miiligan 2007) for both sites (considering the five transition matrices with equal probability). We also estimated quasi-extinction
probabilities (50,000 simulations) for both populations over a 50-year period, when a final mean
population size of 30 individuals was reached. Given
the difficulty and estimation of fecundity, the C1 size
class was excluded from final population densities in
calculating quasi-extinction probabilities (Morris and
Doak 2002).
We simulated changes in particular matrix entries
in the annual projection matrix by changing the
relevant entries in the matrices and directly evaluated
their effect on k. Perturbations were done on three
processes because of the following reasons: (1) the
values of fecundity were changed because seed
germination and seedling establishment (a component
of fecundity) were only estimated and not seen during
the study period within the permanent plots, (2)
growth was identified as having and important effect
on k (according to the values of elasticity), and (3)
survival because this demographic process had the
highest values of elasticity, and the effect of illegal
collection and trade is directly linked to this demographic process. We therefore modified the following
entries: fecundity (matrix entry a1j) growth of the C3
size class (entry a43) and survival of C3, C4, and C5
(matrix entries a33, a44, and a55, respectively). For all
numerical simulations, we changed the relevant
values in the annual matrices and obtained the
stochastic growth rates (ks) after 50,000 simulations
assuming equal probability of occurrence for each
matrix (Morris and Doak 2002).
Owing to the difficulty of estimating fecundity
under natural conditions, we simulated changes (50,
20, 10, and 1% of total seedling survival) in seedling
survival of the mean matrix in order to explore the
influence of successful reproduction on rate of
population growth. The reductions in the estimates
of fecundity were based on the observed seedling
survival rates under field conditions. This analysis
would indicate the effect of different fecundity
probabilities in each population on the population
growth rate. In addition, growth of size class C3 was
increased by 10 and 20%, and stasis in size classes
C3, C4, and C5 was increased by 10 and 20% (to
simulate the protection of adult individuals).

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Results
We found that both sites showed some degree of
human disturbance (DI), but DI differed between
sites. The value of DI for the most disturbed site (S1
site) was 52.05, and 14.71 for the S2 site mainly
related to land degradation and human activities. This
disturbance was also reflected in plant density: mean
density was 90 ind/ha in S1 and 385 ind/ha in S2.
Population dynamics
We found that reproductive individuals do not
produce fruits in successive years. In S2, most
individuals produced fruits in one of the studied
years, while others produced fruits during two or
three consecutive years. No individuals, however,
produced fruits in all five studied years. On the
contrary, reproductive individuals at S1 only produced fruits once over the study period. The
percentage of plants bearing fruits was highly variable between years in S2 (7.71, 9.83, 25.74, 9.7, and
17.81 each year from 1999 to 2004, respectively) and
in S1 plants showed a decreasing fruit production in

Fig. 1 Life cycle diagram


of Mammillaria
huitzilopochtli from two
sites a = S1 and b = S2 in
central Mexico. The values
correspond to the mean
matrix (19992000, 2000
2001, 20012002, 2002
2003, and 20032004). The
numbers in the center of
each circle indicate size
class (C1C5) and stasis.
The average fecundity
(number of seedlings
individual-1 year-1) is
indicated by the lower
hatched arrow connecting
reproductive classes to size
class 1. The solid arrows
connecting circles represent
probabilities of growth and
retrogression between size
classes. Finite rate of
population growth (k SE)
of each site is provided at
the top of each life cycle
diagram

= 0.7733 0.1220
C1

0.125

C2
0.5288

0.0214
0.2226

0.043

C3
0.5042

0.2414

0.1338

C4
0.5646

0.1126

0.0478

C5
0.6464

0.0144

0.0013

0.0008

0.0001

0.0018

= 0.8117 0.1122
C1

0.150

C2
0.3848

b
0.4876

0.0322

C3
0.569

0.245

0.095

C4
0.5484

0.181

C5

0.0908

0.6964

0.0058

0.002

123

four of the five studied years (4.23, 3.78, 0.8, 0, and


5.28 from 1999 to 2004, respectively). Individuals of
the largest size class had lower fruit and seed
production than smaller sized reproductive classes
(4 years in S1, and for 3 years in S2). Even though
mean number of seeds per fruit did not differ between
populations (S1 = 42 23 and S2 = 40 11;
t = 0.17, df = 38, P = 0.864), there were differences in the number of fruits per plant which resulted
in a contrasting total mean seed production by
individual (5.85 2.12 SE seeds/ind for S1 and
23.37 5.24 SE seeds/ind for S2, P \ 0.01). The
germination rate of seeds less than 1-year-old was
95% 2.332 SE in S2 and 89% 0.808 SE in S1,
and the mean seedling survival after 8 months in field
conditions was 12.5% 1.847 SE in S1 and
15% 2.771 SE in S2 (Fig. 1, transition from
seedling to C2). The mean life cycle shows that both
populations begin reproduction at size class C2
(Fig. 1a, b), and stasis increased with size class
except in size class C2 for S1, which showed
important contributions of growth to size class C5
(Table 1). Retrogression from class C3 was observed
at both sites, but at S1 regression to smaller size

0.0034

0.0068

0.0082

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Table 1 Transition matrices by site and year for Mammillaria huitzilopochtli populations

C1

C2

C3

k = 0.8096
0.1535
C4

C1

0.0004

0.0005

0.005

0.002

C2

0.125

0.281

C3

0.351

0.538

0.054

78

C3

0.591

0.318

0.010

217

C4

0.321

0.568

0.040

37

C4

0.429

0.375

104

C5

0.013

0.216

0.760

25

mi

0.875

0.368

0.128

0.162

0.200

S1

20002001

S1

19992000

S2
C5

19992000

ni
0.0079
57

C1

C2

C3

k = 0.7356
0.1534
C4

C5

ni

C1

0.004

0.005

0.009

C2

0.150

0.236

0.017
110

C5

0.375

0.733

mi

0.850

0.173

0.244

0.240

0.267

C5

C1

C2

C3

k = 0.8832
0.1032
C4

C1

0.002

0.005

0.006

C2

0.150

0.731

0.096

45

C1

C2

C3

k = 0.6973
0.1554
C4

C1

0.003

0.001

C2

0.125

0.563

0.156

C3

0.063

0.578

0.447

0.107

64

C3

0.154

0.756

0.235

135

C4

0.031

0.340

0.143

47

C4

0.037

0.561

0.243

132

C5

0.043

0.536

28

74

mi

0.875

0.375

0.234

0.170

0.214

S1

20012002

C5

S2
C5

ni
0.004
16

20002001

C5

0.038

0.595

0.850

0.115

0.111

0.167

0.162

C5

C1

C2

C3

C1

0.0006

0.002

C2

0.125

0.500

C1

C2

C3

k = 0.8366
0.1241
C4

C1

0.008

0.013

0.015

C2

0.150

0.563

0.029

32

C3

0.300

0.435

0.043

62

C3

0.344

0.652

C4

0.355

0.565

23

C4

0.174

0.062

138

0.691

0.082

C5

0.130

0.647

17

C5

0.007

97

0.144

0.653

mi

0.875

0.200

0.210

0.261

0.353

mi

0.850

0.094

49

0.138

0.103

0.265

S1

20022003

C5

C5

S2
ni
0.0026

20012002

C1

C2

C3

k = 0.7338
0.2328
C4

C1

0.003

C2

0.125

0.500

C3

0.200

0.441

34

C3

0.682

0.519

C4

0.324

0.600

35

C4

0.398

C5

0.059

0.143

0.733

15

C5

0.009

mi

0.875

0.300

0.176

0.257

0.267

mi

0.850

0.091

0.065

S1

20032004

C5

C1

C2

C3

k = 0.8742
0.2154
C4

C1

0.0006

0.002

0.0026

C2

0.125

0.800

0.059

C3

0.200

0.529

0.125

C4

0.176

0.750

C5

0.031

mi

0.875

0.235

0.094

0.389

0.037

C1

C2

C3

C1

0.001

0.004

0.002

C2

0.150

0.227

0.009

22

0.042

108

0.547

95

0.295

0.872

47

0.116

0.128

ni
0.003

ni

k = 0.8729
0.1014
C4

S2

10

0.013
26

mi

k = 0.6556
0.5367
C4

20

ni

20022003

ni
0.007

C1

C2

C3

k = 0.7809
0.1422
C4

C1

0.002

0.007

0.009

C2

0.150

0.167

0.027

17

C3

0.667

0.600

0.126

75

0.056

32

C4

0.187

0.568

0.129

95

0.556

18

C5

0.013

0.053

0.629

70

mi

0.850

0.167

0.173

0.253

0.243

S2
ni

20032004

C5

ni
0.018

S1 = population disturbed site; S2 = population conserved site; C1 = seedlings \0.1 cm; C2 = juvenile of 0.12 cm; C3 = young adults of 2.1
4 cm; C4 = mature adults of 4.16 cm; and C5 = old adults of [6 cm, mi = mortality. In the first row, seedlings per class are given. Values in the
main diagonal indicate the probability of stasis, values below the diagonal are transitions corresponding to growth, and values above the diagonal
indicate regression. Instantaneous rates of growth (k SE) are given next to each site 9 year combination. ni is the number of individuals in each size
class

123

60

classes could be found between noncontiguous categories. Mortalities based on the total number of
individuals of the mean matrix were higher in S1 that
in S2 (35.9 and 30.3%, respectively) being variable
between years and sites (mi, Table 1). In both
populations the highest levels of mortality were
predominantly in size class C5, followed by C2 in S1
and C4 in S2 (Table 1).
Growth rates showed declining populations except
in S1 for 20012002 (k = 0.6556 0.5367) and
20032004 (k = 0.8742 0.2154, Table 1). However, the confidence intervals make the value of k at
equilibrium uncertain. The mean matrix showed
values of k below unity for both populations
(Fig. 1) suggesting that over the long term, populations are prone to be in further peril. We found
significant differences between the mean observed
and projected stable size distributions in both populations (Fig. 2, G-test; P \ 0.01). Differences were
mainly found by an excess of observed individuals in
size class C2 and C3 and a more than expected
number of individuals in the last two size classes.
Size classes C1 for both populations and C4 for S1
did not differ from projected stable size distributions.

Fig. 2 Differences between the observed distribution (hatched


bars) and projected stable size (solid bars) of Mammillaria
huitzilopochtli in S1 (black/solid hatch) and S2 = (white/
coarse hatch) habitats. Data were from the mean matrix for
each site from 1999 to 2004. Size classes 15 correspond to the
following (cm): \0.1 (C1, seedlings); 0.12 (C2, juveniles),
2.14 (C3, young adults), 4.16 (C4, mature adults), and [6
(C5, old adults). Asterisks indicate significant differences
between the observed and projected stable size distributions
(P \ 0.05)

123

Plant Ecol (2010) 210:5366

Elasticity analysis
The elasticity analysis on mean annual matrices
showed that the elasticity of stasis was similar for
both sites (S1 = 73.7% and S2 = 75.4%), growth
elasticities were 14.11% and 12.52% for S1 and S2,
respectively, and the elasticity of fecundity was
higher in S2 (13.09%) than in S1 (11.8%). On a
yearly basis, the highest elasticity values corresponded to stasis in some years and to growth in
others suggesting that the populations respond to
precipitation by an increase in the relative importance
of growth (Table 1). In addition, the elasticity of
retrogression was higher at S1 (13.09%) than at S2
(11.8%). In terms of stasis, the highest values were
associated to size category C5 followed by C4 in S1
and by C3 in S2.
Life table response experiments (LTREs)
The LTREs showed different results between populations. In terms of size classes, S2 showed consistent
positive contributions from three out of four size
classes toward k, while in S1 all but size class C4
contributed negatively to k (Fig. 3a). When considering the effect of year (Fig. 3b), the contribution of
C1 was negligible for all years probably due the fact
that entries were estimated; however, contributions
were either consistently negative for size classes C3
or larger (19992000 and 20012002), and the
contributions for the other years are highly variable
between years. When subdividing the contributions
by demographic process, fecundity was consistently
negative for S1 and positive (except during 2000
2001) for S2 (Fig. 4). Stasis contributed negatively in
3 out of 5 years in S1 and 1 out of 5 in S2 (Fig. 4).
For growth, contributions in S1 and S2 tended to have
the same pattern except during 20012002, which
showed positive contributions in S1 and negative in
S2, negative contributions were very high in one year
(20002001, Fig. 4).
Numerical simulations
Mean matrix population growth rate in S1 was below
unity regardless of increases in fecundity, growth or
stasis (Fig. 5). The same decline was found for S2,
except that increases in fecundity above 50% gave
values above unity (Fig. 5). The stochastic growth

Plant Ecol (2010) 210:5366

0.015
0.01

Contributions

Fig. 3 Contribution by a
size class (C1C5) from
analyzing the life table
response experiments
(LTREs) by population
(S1 = white bars and
S2 = black bars), and b by
size class and year (1999
2000 black, 20002001
white, 20012002 gray,
20022003 hatched, and
20032004 dotted), in order
from left to right. Positive
values are associated to
increases in the values
of k, while negative values
are responsible for a
decrease in k

61

0.005
0
-0.005
-0.01
-0.015
C1

C2

C3

C4

C5

Size class

0.03

Contributions

0.02
0.01
0
-0.01
-0.02
-0.03
C1

C2

C3

C4

C5

Size class

rates suggested that both populations are decreasing (S1, ks = 0.7711 0.0004 95% CI, S2, ks =
0.8094 0.0005 95% CI). The quasi-extinction
probability after 6 years was above 0.5 and reached
1 after 9 years for S1, while the population at S2 had
a quasi-extinction probability above 0.5 after
12 years and reached 1 after 17 years.

Discussion
The projected stable size distribution was significantly different from the observed distribution for
both populations as found in other demographic
studies (Rosas and Mandujano 2002; Esparza-Olgun
et al. 2002; Pico and Riba 2002, Godnez-Alvarez
et al. 2003). Interestingly, the reported pattern is
similar: an overrepresentation of the largest size

classes and seedling or juveniles in the stable


structure, suggesting a lack of adults and seedlings
in the observed structure. On the one hand for M.
huitzilopochtli two reasons could determine the
pattern (1) the recent removal of adult individuals
by looting or disturbance and (2) the limiting
conditions imposed by habitat (water runoff, slope,
and bare rock habitat) that contribute to adult
mortality. The main cause of mortality in the largest
size class was associated to dropping of individuals
from the cliffs when their weight can no longer be
supported by the substrate and root system, a size
constraint that is also imposed by habitat conditions.
Garca et al. (2002) also found small numbers of large
individuals in four rupicolous species of the Pyrenees, even though the causes of mortality were not
explored. On the other hand, because seedling
recruitment was not seen during the study period,

123

62

Plant Ecol (2010) 210:5366


F
2003-2004

2002-2003

2001-2002

2000-2001

1999-2000
-0.002

-0.001

0.001

0.002

0.003

2003-2004

Year

2002-2003
2001-2002
2000-2001
1999-2000
-0.2

-0.1

0.1

0.2

0.3

G
2003-2004

2002-2003

Fig. 5 Stochastic log growth rates (log ks) under different


management scenarios in two populations of Mammillaria
huitzilopochtli (S1, black circles and S2, empty circles) in
central Mexico. The matrices used corresponded to five annual
transitions per population (19992000, 20002001, 2001
2002, 20022003, and 20032004), where each matrix had
the same probability of being chosen. Observed value with no
modification from the annual matrices (see Table 1),
SS = fecundity, GC3 = changes in growth for category C3,
S = changes in survival for individuals in size class C4 or C5.
The solid line represents equilibrium conditions (k = 1)

2001-2002

2000-2001

1999-2000
-0.2

-0.15

-0.1

-0.05

0.05

Contributions

Fig. 4 Contributions by demographic process (F = fecundity,


L = stasis and G = growth) from the life table response
experiment (LTRE) for each population (S1 = white bars,
S2 = black bars) and year (20002004). Positive contributions
are associated to increases in the value of k and negative values
to decreases in k

differences observed for size class C2 were probably


due to the fact that our model includes the rate of
recruitment as an estimation, calculated from the
number of seeds (under natural conditions), seed
germination (in controlled conditions), and seedling
survival (under natural conditions). The estimated
probabilities of seedling recruitment and survival for
M. huitzilopochtli are very high (i.e., [0.1) in
comparison to other demographic studies (i.e.,
\0.01, Mandujano et al. 2001, 2007a; Esparza-

123

Olgun et al. 2002; Clark-Tapia et al. 2005; Valverde


and Zavala-Hurtado 2006; Jimenez-Sierra et al.
2007). The method used to estimate recruitment and
seedling survival has been previously used as a
surrogate of fecundity (see Valverde et al. 2004;
Clark-Tapia et al. 2005; Esparza-Olgun et al. 2005);
however, the approach tends to overestimate recruitment. Although the lack of realistic information on
this life cycle transition is a drawback of our data set,
the use of simulations allows an evaluation of their
contributions. In this study, we strongly reduced the
fertility schedule estimated from greenhouse experiments and included a value of fecundity multiplied
by 0.1% as means of adding the realism of field
observations (Mandujano et al. 2001; Contreras and
Valverde 2002).
The simulations and LTREs reinforce the combined importance of seedlings for population growth.
In the Cactaceae, seedling establishment has been
shown to be one of the main bottlenecks to population growth due to the harsh environmental conditions found in arid and semiarid environments
(Shreve 1931; Franco and Nobel 1989; Valiente-

Plant Ecol (2010) 210:5366

Banuet and Ezcurra 1991; Mandujano et al. 2001,


2007a). Almost all demographic studies obtain seed
germination and seedling recruitment from experimental trails (e.g., Esparza-Olgun et al. 2002; ClarkTapia et al. 2005; Jimenez-Sierra et al. 2007). Added
to this difficulty is the fact that the habitat where
M. huitzilopochtli is found contributes to the absence
of seedlings and increases mortality of adults. In
other rupicolous species seedling establishment is
also rare because the natural conditions of these
microhabitats, cracks and cervices of limestone rock
without soil, hard runoff, and high rates of insolation,
strongly reduce the probability of germination and
subsequent survival (Kephart and Paladino1997; Pico
and Riba 2002; Navarro and Guitian 2003; but see
Mungua-Rosas and Sosa 2008). In some cases
seedling establishment was increased by as much as
35% through hand sowing (Garca 2003), a response
also found in M. huitzilopochtli, where hand sowing
in natural conditions increased seedling survival by as
much as 15%.
Our results suggest that given the poor situation of
M. huitzilopochtli and the difficulties for increasing
survival in adult plants, reproduction (recruitment) is
the most practical solution to avoid extinction and
recover a more stable scenario for conservation. The
elasticity values of fecundity were low in all cases,
which is common for perennial plants (Silvertown
et al. 1993; Rosas and Mandujano 2002). Individual
fruit production has no apparent relation to environmental factors (precipitation was similar between the
two studied populations), a phenomenon observed
also in other perennial plants and even in other
rupicolous species (Garca et al. 2002; Pico and Riba
2002; Garca 2003). Variation in flower and fruit
production for cacti species especially for those
inhabiting arid environments has been considered a
bet hedging strategy for the persistence of the
population, as reproductive success can be deferred
to adequate environmental conditions (Bowers 2000)
or pollinator availability. The elasticities were associated to survivorship as found for most Cactaceae
(Rosas and Mandujano 2002; Godnez-Alvarez et al.
2003) but varied in each studied year. The variation
in elasticities is a common result in desert perennial
species (Golubov et al. 1999; Esparza-Olgun et al.
2005; Jimenez-Sierra et al. 2007), which are able to
respond to prevailing environmental conditions.

63

The best estimates of k suggest declining populations but the wide confidence intervals make this
conclusion very uncertain, both populations are
declining with one population tending to increase in
some years. The stochastic growth rate suggests a
dramatic story in which both populations are likely to
go extinct in the near future under current conditions.
The values of k did not correlate with high or low
seed production even though seeds do not generate a
seed bank (Flores-Martnez et al. 2008). Apparently,
perennial species can buffer environmental variation
through the rate of population growth, changing the
relative sensitivities of different demographic processes through time (Mandujano et al. 2001, 2007a;
Esparza-Olgun et al. 2002, 2005; Pico and Riba
2002).
The LTREs showed that contributions of C1
toward k were small compared to other demographic
processes, and a constant negative contribution of
fecundity toward k in all years. However, the
percentage of plants producing seeds in S2 was
always above 6% while plants in S1 had a continuous
decrease in the number of fruits (\5% for all studied
years) a pattern that was followed by all reproductive
categories. It is possible that human disturbance may
be influencing some aspects of reproduction. Being
self-incompatible, with no clonal propagation,
M. huitzilopochtli depends entirely on sexual reproduction (fruit and seeds) and seedling establishment,
two attributes that were more affected at S1, which
had higher disturbance. In rare and threatened species
of cacti, population decreases have been found to be
related to reduced investment in reproduction (Esparza-Olgun et al. 2005; Mandujano et al. 2007b),
which in turn is negatively effected by disturbance
(Jimenez-Sierra et al. 2007; Mandujano et al. 2007a).
The high elasticity values of stasis observed in both
populations suggest that they rely on the survival of
remaining adults, and therefore, population numbers
would decline as these adults disappear. Instead, the
S2 population had the highest elasticity values
associated to growth or stasis depending on the year
indicating a paramount importance of both demographic processes on the rate or population growth.
Under relatively benign conditions, changes in
growth rates affect k more intensely than under
disturbance regimes. If in addition to disturbance
individuals are collected (at a rate of 10% or more for

123

64

the largest size classes) in the disturbed site, populations will decrease over time.
Our results suggest that human disturbance may be
affecting population dynamics. Previous studies
applying the same disturbance technique have shown
that disturbance affects population density of Mammillaria pectinifera (Martorell and Peters 2005). Both
populations of M. huitzilopochtli under current conditions may be lost over time, especially if disturbance is not stopped and a means of increasing
seedling survival is found. The whole species can
only be found in seven sites some of which have
\450 individuals (Peters and Martorell 2000) jeopardizing the success of any recovery plan. The
demographic parameters of this species suggest that
its ability for population growth is severely limited by
a lack of reproduction, which was shown to have
important effects in reproductive populations.
Additionally, the high habitat specificity and small
distribution range of the species are attributes that
further make this species vulnerable to extinction. Few
studies have addressed endangered species in rupicolous habitats (Pico and Riba 2002; Garca et al. 2002;
Garca 2003); so there is little information on their
population dynamics. Specifically for the Cactaceae,
Martorell and Patino (2006) have suggested that some
of the species of the Series Supertextae included in the
Mammillaria (like M. huitzilopochtli and M. crucigera) that are susceptible to chronic disturbance were
once more widely distributed (Martorell and Peters
2005) and are currently restricted to remnant populations (e.g., Pico and Riba 2002). Poor recruitment, the
continuously decreasing fruit and seed production and
high mortality over time could be driving the decline
of M. huitzilopochtli populations. The results of this
study suggest three things: (1) This species is currently
undergoing declining populations. Over longer time
periods, we would expect the decline or extinction of
those populations having small population sizes, no
fecundity and under disturbed habitats; (2) Habitat
conditions are highly restrictive for this species,
limiting seedling survival, establishment of individuals and increasing mortality of adults; and (3) Even
though disturbance cannot be considered to have an
effect on population dynamics it does seems to have
some effect on reproduction and stasis, making the
population rate of increase highly dependent on
survival of individuals rather than other demographic
processes. Several species of the Cactaceae are

123

Plant Ecol (2010) 210:5366

rupicolous, a habitat that is resource limited, unstable,


and patchy that adds to their vulnerability and
conservation status; so the population dynamics of
these species is restricted by demographic behavior,
highly specific habitat requirements in addition to
illegal collection and land use change.
Acknowledgments This research is part of the doctoral studies
of AFM at the Universidad Autonoma MetropolitanaXochimilco (UAM-X) of Mexico under the advice of MMS,
JG. We are grateful to the Cassiano Conzatti Botanical Garden of
CIIDIR IPN Oaxaca for providing the facilities to carry out the
experiments. Permit to collect fruits (SGPA/DGVS/00615) was
granted by SEMARNAT, Mexico. This research was supported
by two CGPIIPN projects (No. 20070431, 20080718) to AFM,
project BBV BIOCON 04-084 CONACyT CB-2006-1 #62390
and CONACyT CB-2007-01 #83790 to JG, project 0350
SEMARNAT-CONACyT
and
PASPA-DGAPA-UNAM
to MCM. We thank I. Rodriguez for field assistance, and
Jeronimo Reyes for locating of populations of M. huitzilopochtli.
This article was written during a sabbatical leave by JG and
MCM at NMSU with B. Milligan who provided logistic support
and helped implementing the popbio package.

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