Herpetologica, 69(4), 2013, 411–435

Ó 2013 by The Herpetologists’ League, Inc.

DEMOGRAPHIC IMPORTANCE OF THE LIFE-CYCLE COMPONENTS

IN SCELOPORUS GRAMMICUS
HIBRAIM A. PÉREZ-MENDOZA1,4, J. JAIME ZÚÑIGA-VEGA1, YAZMÍN H. ZURITA-GUTIÉRREZ1,
JUAN FORNONI2, ISRAEL SOLANO-ZAVALETA3, ANA L. HERNÁNDEZ-ROSAS1, AND
ALEJANDRO MOLINA-MOCTEZUMA1
1
Departamento de Ecologı́a y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México.
Ciudad Universitaria 04510, Distrito Federal, México
2
Departamento de Ecologı́a Evolutiva, Instituto de Ecologı́a, Universidad Nacional Autónoma de México.
Ciudad Universitaria 04510, Distrito Federal, México
3
Departamento de Biologı́a Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México.
Ciudad Universitaria 04510, Distrito Federal, México

ABSTRACT: Survival, growth, and fecundity are considered as the three main components of the life cycle
of any living organism. The relative contribution of these three components to average fitness may vary
drastically among populations of single species. Examining this interpopulation variation and understanding
its causes can provide insight on the particular selection pressures that drive phenotypic divergence among
populations. We conducted a demographic study of eight distinct populations of the viviparous lizard
Sceloporus grammicus in central Mexico. We estimated variation among populations in stage-specific
survival, growth, and fecundity. Using these data we constructed site-specific population projection matrices
to estimate population growth rates, which we interpreted as measures of the average fitness of each
population. Elasticity analysis was used to calculate the relative contribution of the three life-cycle
components to population growth rates. The three life-cycle components had relatively high elasticity values,
which meant that survival, growth, and fecundity contributed similarly to fitness. However, some variation
was found among populations. We searched for potential associations between the observed interpopulation
variation in these measures of relative importance for average fitness and interpopulation variation in
temperature, rainfall, population density, microhabitat availability, degree of human-induced disturbance,
and overall mortality. None of these environmental factors or their interactions could explain the observed
interpopulation variation in the relative importance of the life-cycle components. Our results provide insight
about how these viviparous lizards allocate resources to survival, growth, and fecundity in different
environments.
Key words: Elasticity analysis; Fast–slow continuum; Life-history evolution; Mark–recapture experiment;
Projection matrices

DIFFERENT populations of a species may contribution of the three main components of

experience drastically different demographic
processes. For example, individuals inhabiting
different localities usually experience different
vital rates (age-specific survival and fecundity
schedules, age at first reproduction, body
growth rates, etc.), resulting in population
growth rates that can differ in magnitude or
direction (Oliveira and Rinaldi, 2003). This
spatial variation results from different selec-
tive regimes that promote interpopulation
variation in demographic and life-history
strategies (Forsman and Shine, 1995). The
ecological and evolutionary impact of such
interpopulation differences in the vital rates
can be analyzed by estimating the relative
4
CORRESPONDENCE: e-mail, hibraimperez@ciencias.
unam.mx
the life cycle (fecundity, growth, and survival)
to the intrinsic rate of population growth (k;
Franco and Silvertown, 1996). Population
growth rates have been interpreted as mea-
sures of the average fitness of populations
(Benton and Grant, 1999; Metcalf and Pavard,
2007). Previous studies have shown that
populations may vary widely in the relative
importance of fecundity, growth, and survival
rates for their persistence probabilities (Gail-
lard et al., 2000). Exploring these intraspecific
differences can reveal selection pressures that
drive phenotypic divergence among popula-
tions including variation in morphological,
physiological, behavioral, demographic, and
life-history traits.
Several biotic and abiotic factors can
promote differences among populations in
the age- or stage-specific vital rates and, in

411
412 HERPETOLOGICA
turn, in the relative importance of fecundity,
growth, and survival for average fitness
(Boutin and Harper, 1991; Stearns, 1992;
Caswell, 2001; Angilleta et al., 2004). With
respect to the biotic environment, population
density has proven to be a strong selective
factor affecting vital rates with relatively slow
body growth, low survival, and decreased
fecundity under dense conditions (Reznick
et al., 2002, and literature therein). With
respect to the abiotic environment, tempera-
ture and rainfall can also affect vital rates with
relatively slow body growth, low survival, and
decreased fecundity under arid conditions
(dry and extremely warm; Niewiarowski,
2001; Sinervo et al., 2010). In addition,
microhabitat availability and the degree of
human-induced disturbance may also affect
the vital rates. Low microhabitat availability or
a high degree of disturbance may promote
reduced growth, survival, or fecundity (Ruh-
len et al., 2003; Rittenhouse, 2008); however,
some species actually increase their fitness in
disturbed environments (e.g., Smart et al.,
2005). When the rates of body growth are slow
and fecundity is limited, the contribution of
these vital rates to the rate of population
growth is small and, therefore, the survival of
individuals is the life-cycle component that
makes the greatest contribution to the persis-
tence of populations. Therefore, this demo-
graphic pattern is the expected outcome in
extremely arid environments, in sites with
high population density, with low microhabitat
availability, or with a high degree of distur-
bance. In contrast, when individuals exhibit
fast rates of body growth and increased
fecundity, the contribution of these life-cycle
components to the rate of population growth
is high because maturity can be reached early
in life and many offspring are produced
(Silvertown et al., 1992; Heppell et al., 2000;
van Tienderen, 2000; Franco and Silvertown,
2004). This latter demographic pattern is
expected in mesic environments, in sites with
low population density, with high microhabitat
availability, or with moderate or null human-
induced disturbance.
In addition, extrinsic mortality, independent
of its cause, has also been related to the
relative importance of the life-cycle compo-
nents. Species and populations experiencing
[Vol. 69, No. 4
low mortality rates appear to evolve slow body
growth, decreased fecundity, and a large
contribution of the survival of individuals to
their average fitness. In contrast, species and
populations experiencing high mortality rates
appear to evolve fast body growth, increased
fecundity, and a large contribution of these
two processes to their average fitness (Gadgil
and Bossert, 1970; Promislow and Harvey,
1990; Johnson and Zúñiga-Vega, 2009). In
fact, these relationships between extrinsic
mortality and the relative importance of
fecundity, growth, and survival for average
fitness have been considered as evidence
supporting the fast–slow continuum hypothe-
sis of life-history evolution (Promislow and
Harvey, 1990; Franco and Silvertown, 1996;
Oli, 2004). Under this theoretical model,
extrinsic mortality is a strong selective factor
shaping the relative speed of the life cycle and
the amount of reproductive investment. Fast
life cycles with a high contribution of fecun-
dity and growth to average fitness should
occur in high-mortality environments whereas
slow life cycles with a high contribution of
survival to average fitness should occur in low-
mortality environments. Most studies provid-
ing evidence for this hypothesis have focused
on interspecific comparisons (Gaillard et al.,
1989; Promislow and Harvey, 1990; Black-
burn, 1991; Franco and Silvertown, 1996;
Bauwens and Dı́az-Uriarte, 1997; Clobert et
al., 1998; Heppell et al., 2000; Sæther and
Bakke, 2000; Oli and Dobson, 2003). Studies
testing this theoretical model with different
populations of single species inhabiting con-
trasting environments are, by far, less com-
mon (Miller et al., 2011).
In this study we tested these predictions
with the viviparous lizard Sceloporus grammi-
cus. This species is widely distributed
throughout central Mexico and is abundant
in most of the sites which it inhabits (Sites et
al., 1992). However, little is known about the
different demographic processes (i.e., differ-
ent mortality, birth, and body growth rates)
that occur in different populations (Zúñiga-
Vega et al., 2008a). For these reasons, this
species is an ideal model to understand the
ecological and evolutionary impacts of the
demographic processes occurring in different
populations. We were particularly interested
December 2013] HERPETOLOGICA
in the causes and consequences of differences
in the relative importance of fecundity,
growth, and survival for average fitness.
The main objective of our study was to
analyze the population dynamics of different
populations of S. grammicus, focusing on
intraspecific variation in stage-specific vital
rates, in the rates of population growth, and in
the relative contribution of the life-cycle
components (survival, growth, and fecundity)
to average fitness. We also explored potential
associations of rainfall, environmental temper-
ature, aridity, population density, microhabitat
availability, degree of human-induced distur-
bance, and overall mortality with the vital
rates and with the relative contribution of the
life-cycle components to average fitness.
MATERIALS AND METHODS
Study Species
Sceloporus grammicus is a viviparous lizard
widely distributed in Mexico; it ranges from
southern Texas through most of mainland
Mexico (Arévalo et al., 1991). Mean size is
approximately 64 mm snout–vent length
(SVL; Canseco-Márquez and Gutiérrez-May-
en, 2010). In some populations males reach
sexual maturity at 6 or 7 mo of age whereas
females do so at 8 or 9 mo (Jiménez-Cruz et
al., 2005). Females of S. grammicus only
produce one litter per year (Guillette and
Bearce, 1986). According to the literature,
births occur during April in central Mexico,
although we have recorded births as early as
mid-February. Litter sizes have been docu-
mented to vary among populations between
2–10 offspring per female (Ramirez-Bautista
et al., 2005). There is a positive correlation
between female size and number of offspring
(Jiménez-Cruz et al., 2005). Because of its
wide geographic distribution, there is large
variation in ecological, morphological, and
genetic (there are eight known chromosomal
races) traits of this species (Sites and Green-
baum, 1983; Arévalo et al., 1993, 1994).
Study Sites and Field Methods
We studied eight populations of S. grammi-
cus in the states of Hidalgo, Tlaxcala, and
Queretaro in central Mexico (Fig. 1). We
followed two main criteria to select our study
sites. First, the study sites had to differ in
413
environmental conditions such as vegetation
type, total annual rainfall, mean temperature,
types of microhabitats in which lizards can be
found, microhabitat availability, and degree of
human-induced disturbance (Table 1). In this
way we maximized the probability of observ-
ing distinct vital rates among populations, and
we were able to search for associations
between environmental conditions and vital
rates in our attempt to understand the factors
that drive intraspecific differences in fecundi-
ty, growth, and survival of these lizards.
Second, we needed sites where S. grammicus
was abundant enough to secure samples sizes
that were large enough to yield robust and
precise estimates of demographic parameters.
We recognize that some sites are geograph-
ically close to each other (Fig. 1). However, in
all cases at least some of the factors that we
examined, such as lizard population density,
vegetation assemblages, microhabitat avail-
ability, or degree of disturbance, differed
between such close populations. This means
that selective pressures differed between all
pairs of populations, regardless of geographic
proximity. For example, populations 4 and 5
separated by only 10.6 km but population
density of these lizards and microhabitat
availability were markedly different between
these two sites (Table 1).
At each study site we delimited a single
study plot in which lizards were relatively
abundant; by abundant we mean that we
could capture at least 20 lizards per sampling
occasion. Hence, we determined the size of
the study plots as the minimum area required
to capture at least 20 lizards during a working
day. Given that each study site constitutes a
different set of conditions, which result in
distinct population densities of S. grammicus
or in different chances of capturing a lizard,
some study plots were larger than others (Site
1 was the largest and Site 5 was the smallest;
Table 1). We conducted mark–recapture
experiments at these sites from July of 2009–
November of 2011. During this period we
visited the populations approximately once
every 2 mo. However, due to logistic reasons,
the total number of visits varied among
populations (between 11 and 13; Table 1).
On each visit we searched for lizards from
0900 to 1800 h. During this time we
414 HERPETOLOGICA [Vol. 69, No. 4

FIG. 1.—Geographic location of the study populations of the viviparous lizard Sceloporus grammicus. Numbers were
assigned to sites according to the Reichel’s aridity index: from the most-arid site (1) to the least-arid site (8). The datum
for geographic coordinates was WGS84, with Lambert conformal conic projection.

attempted to capture as many lizards as
possible. Individuals were captured by hand
or noose. Upon first capture, individuals were
marked individually by clipping toes following
the Waichman (1992) code. On each capture
the following information was recorded for
each individual: sex, body mass, and snout–
vent length (SVL). Sex was ascertained by
examination of the postanal scales (enlarged in
males). Individuals were released immediately
after these measurements were taken. Re-
peated visits to the study sites allowed us to
record individualized encounter (recapture)
histories which consisted of data on when
lizards were seen or not seen over the course
of the study.
We recognized that our studied populations
might exhibit genetic differences. Previous
evidence indicated distinct chromosomal rac-
es within S. grammicus (Arévalo et al., 1993).
We identified the most-likely chromosomal
race for each study site according to the
proximity to other populations for which the
chromosomal race has already been accurately
described (Arévalo et al., 1994; Table 1).
Given the potential genetic differences among
our studied populations, we recognized that
part of the differences or similarities among
sites that we report here regarding vital rates
might be explained by historical gene flow or
shared evolutionary (phylogeographic) history.
Therefore, we interpreted our results with the
appropriate level of caution. However, several
studies have demonstrated that demographic
traits (survival, growth and recruitment rates)
are shaped predominantly by the local envi-
ronment rather than by genetic similarities
among populations (Via, 1999; Svensson and
Sinervo, 2000; McKay et al., 2001). This is the
main assumption that underlies the present
study.
TABLE 1.—Description of the eight study populations of the viviparous lizard Sceloporus grammicus. We report mean annual rainfall, mean annual temperature, and the
December 2013]

Reichel’s aridity index (IR). We classified these sites according to the relative availability of microhabitats (low versus high) as well as according to the degree of human-induced
disturbance (wild areas, agriculture lands, and urban areas). The putative chromosomal race of each population, the area of each study plot, and the total number of visits to
each study site are also shown.

Putative
Site Geographic location, Degree of human- Microhabitat Temperature chromosomal Study plot Total number
numbera elevation (MAMSL) Vegetation type induced disturbance availability Rainfall (mm) (8C) IR raceb area (ha) of visits

1 20847 0 0.42 0 0 N Shrubland Wild area Low 511 16.04 1398.12 F5þ6 9.97 12
99843 0 10.25 0 0 W
2198
2 20816 0 6.74 0 0 N Shrubland Wild area High 549 15.13 1438.86 F5þ6 or 0.84 12
99838 0 26.23 0 0 W FM1
2489
3 19847 0 56.10 0 0 N Nopalera (Opuntia spp. Agriculture land High 435 13.89 1636.16 FM2 0.32 13
98832 0 57.00 0 0 W forest)
2473
4 208 2 0 36.32 0 0 N Agriculture land Agriculture land Low 519 15.12 1713.77 FM2 0.24 12
98837 0 10.40 0 0 W
2525
5 208 1 0 47.59 0 0 N Agriculture land Agriculture land High 540 15.03 1818.82 FM2 0.11 12
HERPETOLOGICA

98831 0 35.31 0 0 W
2604
6 19833 0 30.83 0 0 N Urban area with Junipers Urban area Low 673 14.16 2704.15 S 0.60 12
98813 0 22.00 0 0 W and shrubland elements
2583
7 19838 0 19.68 0 0 N Urban area with junipers Urban area Low 693 14.03 2802.53 S 0.06 11
988 6 0 55.15 0 0 W
2708
8 19811 0 20.56 0 0 N Agriculture land Urban area High 822 14.26 3251.24 S 0.09 13
97855 0 23.56 0 0 W
2629
a
Numbers were assigned to sites according to the aridity index: from low to high IR values (from more to less arid). These numbers identify sites throughout the text.
b
F ¼ Fission. The following numbers are the number of chromosomes which probably were divided. F5þ6 has a 2n¼36; M ¼ Multiple. This indicates that this chromosomal race has probably suffered multiple fissions. FM1 has a
2n¼40-42, whereas FM2 has a 2n¼44-46; S ¼ Standard. This is the standard chromosomal race and has a 2n¼36.
415
416 HERPETOLOGICA [Vol. 69, No. 4

TABLE 2.—Minimum size at maturity, threshold size that separates small adults from large adults, total sample sizes per
stage class, and estimates of population density for the study populations of the viviparous lizard Sceloporus grammicus.

Size at maturity Threshold size for Sample sizesb

(mm snout– adult stage classes Population density
Sitea vent length) (mm snout–vent length) J SA LA (lizards/m2)

1 46.02 61.33 19 (4) 74 (20) 5 (2) 0.001

2 44.69 59.21 97 (10) 182 (41) 16 (2) 0.03
3 46.00 59.12 83 (14) 161 (45) 4 (2) 0.04
4 48.03 55.17 84 (15) 74 (34) 14 (7) 0.05
5 44.02 50.03 147 (33) 130 (36) 65 (33) 0.18
6 54.24 67.09 100 (21) 122 (34) 11 (1) 0.03
7 55.00 65.28 72 (9) 20 (6) 3 (1) 0.11
8 49.23 70.04 45 (7) 87 (33) 16 (4) 0.13
a
Numbers were assigned to sites according to the aridity index: from low to high IR values (from more to less arid). These numbers identify sites throughout
the text.
b
J ¼ juveniles; SA ¼ small adults; LA ¼ large adults. The number of lizards that were recaptured at least once during the study period is shown within
parentheses.

Estimating Stage-specific Survival, Recapture,
and Transition Rates
The eight studied populations were struc-
tured into three size–stage classes. Juveniles
were all those lizards smaller than the site-
specific minimum size at maturity (Table 2).
Small adults were all those reproductive
individuals still exhibiting measurable body
growth (we calculated body growth rates as
per Zúñiga-Vega et al., 2008b). Large adults
were all those reproductive individuals whose
rates of body growth were negligible. For each
population, we estimated the minimum size at
maturity as the SVL of the smallest pregnant
female (determined by palpation; Table 2).
The threshold size between small and large
adults corresponded to the site-specific SVL at
which we began to register rates of body
growth that were close to zero (,0.0001 mm/
d; as per Zúñiga-Vega et al., 2008b; Table 2).
Hence, individuals considered as large adults
were all those that apparently did not grow
between consecutive capture occasions. We
assumed that such large adults reached their
asymptotic size and, therefore, did not allocate
resources or energy to body growth but only
to reproduction and maintenance. For these
three categories and for the eight studied
sites, we estimated annual probabilities of
survival, recapture, and transition (i.e.,
growth) between stage classes.
The encounter histories were used as input
in the program MARK to calculate stage-
specific survival, recapture, and transition
rates through a multi-state framework
(Brownie et al., 1993; White and Burnham,
1999). MARK uses maximum-likelihood rou-
tines to estimate two main parameters:
survival (u) and recapture (p) probabilities
(Lebreton et al., 1992). Multi-state analyses
also calculate the transition (growth) rate from
one state (in our case from any stage class) to
another (w). MARK provides the values of
these parameters that maximize the probabil-
ity of obtaining the observed encounter
histories (White and Burnham, 1999).
Model Set
We used a multi-model inference frame-
work (Burnham and Anderson, 2002) to
examine variation in survival, recapture, and
transition rates. For each population we
defined a candidate model set where u, p,
and w could either be constant (.) or vary
among stage classes (sc) or sampling occasions
(i.e., time-dependent ¼ t). Following our
predictions, we also considered the possibility
that u, p, and w could depend on population
density. Hence, we included an estimate of
population density per sampling occasion (d)
as another source of variation for these
parameters. Occasion-specific population den-
sity (di) was estimated as ni/pi, where ni is the
number of captured lizards at each sampling
occasion i and pi is the estimated capture
probability at occasion i (Armstrong et al.,
2005; Zúñiga-Vega et al., 2011). We did not
consider the interactions among stage class,
sampling occasion, and population density as
sources of variation for u, p, and w because
December 2013] HERPETOLOGICA 417

Table 3.—Results of fitting competing models that represented different sources of variation for the survival (/),
recapture (p), and transition (w) rates to the mark–recapture data of eight populations of the viviparous lizard
Sceloporus grammicus.

Sitea Modelb AICc DAICc wi

1 u(.) p(.) w(sc) 283.40 0 0.57

u(sc) p(.) w(sc) 286.78 3.38 0.11
2 u(d) p(sc) w (t) 563.08 0 0.86
u(sc) p(.) w(.) 571.38 8.30 0.01
3 u(.) p(sc) w (sc) 824.24 0 0.29
u(d) p(t) w (sc) 824.40 0.15 0.27
u(.) p(t) w (sc) 824.55 0.31 0.24
u(d) p(sc) w (sc) 826.35 2.11 0.10
4 u(sc) p(t) w (sc) 633.05 0 0.73
u(.) p(t) w (sc) 636.24 3.20 0.15
5 u(.) p(.) w (sc) 1041.09 0 0.27
u(.) p(sc) w (sc) 1041.19 0.10 0.26
u(.) p(d) w (sc) 1042.84 1.75 0.11
u(d) p(.) w (sc) 1042.88 1.79 0.11
u (d) p(sc) w (sc) 1043.13 2.04 0.10
6 u (d) p(sc) w (d) 630.32 0 0.39
u (sc) p(sc) w (d) 630.82 0.50 0.30
u (.) p(sc) w (.) 633.16 2.84 0.09
7 u(.) p (sc) w(.) 188.09 0 0.14
u(d) p(sc) w(.) 188.57 0.49 0.11
u(.) p (d) w(.) 188.87 0.78 0.09
u(.) p(d) w(sc) 189.17 1.08 0.08
u(.) p (sc) w(sc) 189.34 1.25 0.08
u(d) p(sc) w(sc) 189.99 1.90 0.05
u (.) p (.)w (.) 190.50 2.42 0.042
8 u(d) p(sc) w (sc) 523.72 0 0.18
u(d) p(sc) w (.) 524.01 0.29 0.15
u (sc) p(d) w (sc) 524.75 1.03 0.11
u (sc) p(d) w (.) 524.89 1.17 0.10
u (sc) p(d) w (d) 525.26 1.54 0.08
u (d) p(sc) w (d) 525.82 2.10 0.06
a
Numbers were assigned to sites according to the aridity index: from low to high IR values (from more to less arid). These numbers identify sites throughout
the text.
b
Survival (/), recapture (p), and transition (w) rates may vary among stage classes (sc), among sampling occasions (t), as a function of population density (d),
or may be simply constant (.) among stages and sampling occasions. The fit of each model to the observed data was evaluated using a corrected version of the
Akaike’s Information Criterion (AICc). The model with the lowest AICc score best fitted the data. For each population, models are listed according to the AICc
(from lowest to highest, from best to worst). DAICc represents the difference in AICc values between the corresponding model and the best-fitting model.
Models with DAICc ,2 are considered to have support comparable to the best model. Akaike weights (wi) measure the relative support in the data for each
fitted model. Only the models with the strongest support are shown for each study site.

calculating different parameters for all the
possible combinations of these factors would
have required larger sample sizes than those
available to us. In total, we fitted 64 compet-
ing models to our mark–recapture data sets
using maximum likelihood routines in MARK.
Given that sampling dates and number of
sampling occasions differed among sites, we
analyzed separately the mark–recapture data
of each population.
The best-fitting model was selected using
the Akaike Information Criterion (AIC),
which is a measure of model likelihood and
parsimony (Akaike, 1973; Burnham and An-
derson, 2002). Specifically, we used a correct-
ed version of the AIC (AIC c ) that is
appropriate for small sample sizes (Burnham
and Anderson, 2004). The smallest value of
the AICc indicates the model that best fits the
data (Table 3) with the lowest possible
number of parameters. A difference between
models in AICc values (DAICc) larger than 2
indicates a real difference in their fit to the
mark–recapture data (Burnham and Ander-
son, 2002). We also calculated model-specific
Akaike weights (wi), which measure the
relative support or weight of evidence for
each model in the data (Amstrup et al., 2005).
Based on these wi values it was possible to
calculate, for each population, weighted aver-
 418 HERPETOLOGICA [Vol. 69, No. 4

(0.27)
(0.88)
(0.37)
(1.57)
(0.29)
(0.95)
(0.84)
(0.41)
ages for the annual survival, recapture, and
TABLE 4.—Annual estimates of stage-specific survival (u), recapture (p), transition (w), and fecundity rates for eight populations of the viviparous lizard Sceloporus grammicus.
Annual estimates of u, p, and w correspond to model-weighted averages (see text for details). The number of pregnant (captive) females with which we estimated annual

transition rates of individuals in the different

LA
Average number of
offspring produced

3.33
4.14
3.50
6.67
4.34
3.94
3.50
4.20
stage classes as per Burnham and Anderson
(2002). These model-weighted estimates of u,
(0.27)
(1.53)
(0.37)
(0.97)
(0.29)
(0.95)
(0.84)
(0.41)
p, and w incorporate the uncertainty in the
process of model selection by considering the
SA

3.33
2.57
3.50
4.00
4.34
3.94
3.50
4.20
relative support for each competing model.
Therefore, these weighted-average estimates
are more robust than those derived from any
pregnant females

LA

1
5
2
4
7
5
2
2
Number of

single model alone (Johnson and Omland,

2004).
22
5

11
9
2
2

2
3
SA

We must emphasize that, for each popula-

tion and for each stage class, we used our
(0.03)
(0.03)
(0.02)
(0.04)
(0.03)
(0.05)
(0.08)
(0.02)

multi-occasion mark–recapture data to calcu-

Numbers were assigned to sites according to the aridity index: from low to high IR values (from more to less arid). These numbers identify sites throughout the text.
w SA–LA

late weighted-average annual values of u and

0.09
0.04
0.04
0.11
0.11
0.07
0.07
0.05
fecundity is also shown. Standard errors are shown within parentheses.

w. However, we tested for different sources of

variation in u, p, and w, including time
0.03 (, 0.001)

(0.09) , 0.001 (, 0.001)

dependency (i.e., parameters varying among

0.04 (0.03)
0.002 (0.02)
0.007 (0.03)

0.06 (0.05)
0.04 (0.05)
0.03 (0.01)

sampling occasions), because we aimed to

w J–LA

obtain the best average estimates of these

rates while accounting for potential within-site
variation. In this way, data for several
sampling occasions during two complete years
(0.08)
(0.05)
(0.14)
(0.11)

(0.06)
(0.07)
(0.04)

allowed us to calculate robust, reliable, and

w J–SA

accurate site- and stage-specific annual pa-

0.78
0.04
0.32
0.35
0.45
0.08
0.09
0.07

rameters. Site- and stage-specific annual

mortality was calculated simply as 1  u.
(0.03)
(0.11)
(0.13)
(0.13)
(0.04)
(0.03)
(0.14)
(0.06)

Estimating Fecundity Rates

p LA

0.11
0.15
0.24
0.20
0.21
0.02
0.21
0.20

Annual fecundity was estimated by captur-

ing pregnant females from the study popula-
(0.02)
(0.06)
(0.09)
(0.13)
(0.03)
(0.04)
(0.15)
(0.04)

tions, but from outside of the study plots,

p SA

during February, March, and April of 2011.

0.11
0.13
0.25
0.20
0.18
0.18
0.31
0.18

Captured females were maintained in the

laboratory in individual cages. Food and
(0.05)
(0.07)
(0.11)
(0.13)
(0.06)
(0.03)
(0.10)
(0.04)

water were provided ad libitum. Parturitions

pJ

occurred during February, March, April,

0.09
0.06
0.16
0.20
0.22
0.09
0.18
0.04

May, and June of this same year. For each

female we recorded number and size (SVL
(0.05)
(0.24)
(0.18)
(0.18)
(0.06)
(0.36)
(0.21)
(0.12)

J ¼ juveniles; SA ¼ small adults; LA ¼ large adults.

and body mass) of offspring. Females and

u LAb

their offspring were then released in their

0.59
0.25
0.19
0.29
0.22
0.54
0.17
0.30

corresponding populations. Using these data

we calculated an average annual number of
(0.05)
(0.23)
(0.17)
(0.19)
(0.05)
(0.13)
(0.21)
(0.10)
u SAb

offspring per female for both reproductive

0.56
0.26
0.19
0.49
0.22
0.27
0.18
0.40

stages (small and large adults). Recall that

females of this species have only one
(0.05)
(0.24)
(0.18)
(0.19)
(0.06)
(0.35)
(0.18)
(0.08)

reproductive event per year (Guillette and

u Jb

Bearce, 1986). Sample sizes for estimating

0.65
0.24
0.20
0.14
0.22
0.51
0.16
0.24

fecundity (i.e., number of pregnant females

that were kept in captivity) are shown in
Sitea

Table 4.
a
1
2
3
4
5
6
7
8
December 2013] HERPETOLOGICA
Potential Associations between Vital Rates and
Environmental Factors
To examine potential effects of precipitation
and temperature on the stage-specific vital
rates (survival, growth, and fecundity) of S.
grammicus, we obtained climate data from
meteorological stations (Servicio Meteor-
ológico Nacional – México) that were located
close to our study sites. We used two different
approaches to test for the effects of precipi-
tation and temperature on the vital rates. Our
first approach attempted to account for short-
term (year-to-year) variability in both rainfall
and temperature. Specifically, we examined if
the years during which we conducted this
study (2009–2011) were warmer, colder,
rainier, or drier than usual. For this purpose
we calculated site-specific residual values of
rainfall and temperature for the studied years
with respect to the site-specific average values
of rainfall and temperature for the last 20 yr.
These residuals were simply calculated as the
difference between the observed values of
rainfall and temperature during the studied
years and the historical average of these
environmental factors (for the last 20 yr). A
positive residual indicated a warmer- or
rainier-than-average year. A negative residual
indicated a colder- or drier-than-average year.
In addition, we also accounted for potential
autocorrelation in rainfall and temperature
(i.e., for trends across the years that may
obscure important year-to-year changes;
Pyper and Peterman, 1998). For this purpose
we fitted first-order autoregressive models (as
per Box et al., 2008) to the 20-yr data of
rainfall and temperature. We found a signif-
icant effect of past values on subsequent
values (i.e., significant autoregressive models)
for mean annual temperature of Site 8 (F1,18 ¼
22.41, P ¼ 0.0002) and for total annual rainfall
of Sites 3 and 7 (F1,18 ¼ 6.47, P ¼ 0.02; F1,18 ¼
9.28, P ¼ 0.007, respectively). Therefore, for
these particular sites and environmental
variables we obtained residuals from these
significant autoregressive models instead of
residuals from the historical average. Residu-
als that are free of autocorrelation also
indicated if our studied years had higher or
lower values for rainfall or temperature but, in
this case, with respect to the interannual
trends that we detected in these particular
419
populations (Pyper and Peterman, 1998). We
searched for significant associations between
site-specific residual values of rainfall and
temperature and the site- and stage-specific
vital rates of S. grammicus by means of
pairwise Spearman Correlations. According
to our predictions, we expected positive
correlations between residuals of rainfall and
the stage-specific vital rates of S. grammicus
with relatively high growth, survival, and
fecundity rates in sites with higher-than-usual
rainfall. In contrast, we expected negative
correlations between residuals of temperature
and the vital rates with relatively low growth,
survival, and fecundity rates in warmer-than-
usual sites.
Our second approach attempted to account
for spatial (interpopulation) variability in both
rainfall and temperature. For this purpose we
calculated an aridity index for each popula-
tion. Aridity indexes are quantitative indica-
tors of the degree of water deficiency present
at any given location and typically express the
combined effects of precipitation and tem-
perature (Ranjan et al., 2006). Our studied
sites were located in arid or semi-arid
environments (Table 1), and lizards living
under these conditions are particularly sensi-
tive to water loss and extreme temperatures
(Munsey, 1972; Mautz, 1980; Zucker, 1980).
In particular we used Reichel’s Index (IR,
Reichel, 1928), which is a modification of the
De Martonne’s (1926) Aridity Index. We used
this index because it accounts for the number
of days with rainfall, thereby incorporating an
indirect estimate of the amount of time that
lizards can remain active (during rainy days
these lizards remain hidden; Pérez-Mendoza,
personal observation). In ectotherms, activity
time is directly associated with survival
probability given that predation-driven mor-
tality is minimal when individuals are inactive
(Rose, 1981; Adolph and Porter, 1993). Thus,
survival rates might depend to some extent on
the number of days with rainfall. Reichel’s
index was calculated as:
NP
IR ¼
T þ 10
where N is the number of days with rainfall, P
is mean annual precipitation, T is mean annual
temperature, and 10 is a correction factor (the
420 HERPETOLOGICA
addition of 10 degrees to mean temperature
corrects for negative 8C). We used the
historical average of these environmental
factors (for the last 20 yr) to calculate IR for
each population. As with the De Martonne’s
Index, low IR values indicate more aridity (low
water availability) whereas large values indi-
cate less aridity (high water availability).
Notice that in Table 1 numbers were assigned
to sites according to the aridity index (i.e.,
from low to high IR values, from more to less
aridity). We also searched for significant
associations between site-specific IR values
and the site- and stage-specific vital rates of S.
grammicus by means of pairwise Spearman
Correlations. We expected positive correla-
tions between vital rates and IR values, with
increased survival, growth, and fecundity in
mesic sites.
In addition to testing the effects of rainfall
and temperature on the vital rates of S.
grammicus, we also tested for the potential
effect of different population densities among
study sites. For this purpose, we calculated
average density per population across all
sampling occasions. Similarly to the effects
of rainfall and temperature, we searched for
significant associations between site-specific
population density and the site- and stage-
specific vital rates of S. grammicus by means
of pairwise Spearman Correlations. According
to our predictions, we expected negative
correlations between site-specific population
density and stage-specific survival, growth,
and fecundity rates.
To examine the potential influence of
microhabitat availability on the stage-specific
vital rates of S. grammicus, we classified our
study sites into two categories: low and high
microhabitat availability (Table 1). The crite-
rion to distinguish between high and low
microhabitat availability was the number of
potential refuges or perch sites for these
lizards. Given that these refuges or perch
sites may be trees, cacti, or walls of houses, we
simply counted these in our study plots and
arbitrarily determined whether they were
relatively abundant or scarce with respect to
the size of the corresponding study plot. The
cutoff value between sites with low and high
microhabitat availability was an average of one
refuge or perch site per 100 m2. The mean
[Vol. 69, No. 4
number of potential refuges per 100 m2 for
our sites with low microhabitat availability was
0.62 6 0.19 (mean 6 SE), whereas that for
our sites with high microhabitat availability
was 2.17 6 0.69. We tested for differences in
the stage-specific vital rates between low and
high microhabitat availability by means of
Mann–Whitney U-tests. We expected signifi-
cantly higher survival, growth, and fecundity
rates in sites with relatively high microhabitat
availability.
Similarly, to examine the potential influence
of the degree of human-induced disturbance
on the stage-specific vital rates of S. grammi-
cus, we classified our study sites into three
categories: wild areas (where there are no
flora or fauna associated with human activi-
ties), agriculture lands (where cultivated
plants dominate the landscape), and urban
areas (where the landscape has been modified
by houses or buildings; Table 1). We tested for
differences in the stage-specific vital rates
among wild areas, agriculture lands, and
urban areas by means of Kruskal–Wallis tests.
We expected significantly higher survival,
growth, and fecundity rates in sites without
human-induced disturbance (wild areas) com-
pared to agriculture lands or urban areas.
Given that all the environmental factors that
we studied might interactively affect the vital
rates of S. grammicus (e.g., the combination of
the highest population density and the most
arid conditions might promote the lowest
survival, growth, and fecundity rates), we
tested for significant effects of two-way
interactions between population density, rain-
fall residuals, temperature residuals, aridity,
and microhabitat availability on the site- and
stage-specific vital rates of S. grammicus. For
this purpose we constructed linear models
characterized by different combinations of
two of these factors affecting each of the
stage-specific vital rates. Given that our
sample size was limited (eight populations),
we did not test for the effects of interactions
among three or more environmental factors
(more degrees of freedom are needed to test
three-way interactions). Moreover, we did not
test for the effects of interactions between
degree of human-induced disturbance and all
other factors because we had only two
populations (two data points) in the category
December 2013] HERPETOLOGICA
‘‘wild areas’’ (Sites 1 and 2; Table 1). To meet
the assumptions of these models, we applied
the arcsine transformation to all survival and
transition rates and a logarithmic transforma-
tion to fecundity rates (Zar, 2010).
Matrix Population Models
We used projection matrices (Caswell,
2001) to analyze population dynamics. Given
that we structured our populations in 3 size–
stage classes, we constructed 3 3 3 stage-
structured matrices. For each population we
constructed only one average annual matrix
using the estimated annual survival, transition
(growth), and fecundity rates. Matrix entries
represent all the transitions and contributions
that can be observed among stage classes from
one year to the next. When lizards survive
they can either remain in the same stage class
(permanence, P) or progress to a larger stage
class (growth, G). Both adult categories
contribute to juveniles by means of fecundity
(F). Hence, matrix entries (aij) represent the
probability of survival with permanence (in
the main diagonal), the probability of survival
with growth (in the sub-diagonals), and the
contribution to juveniles through fecundity (in
the first row) of an average individual in stage
class j (columns) to stage class i (rows) from
one year to the next (Caswell, 2001).
Permanence and growth entries were de-
rived from the annual survival (u) and
transition (w) rates estimated by program
MARK (Lebreton et al., 1992; Nichols et al.,
1992). Usually projection matrices are con-
structed using only female data (Caswell,
2001). However, when we tested for differ-
ences between sexes in both u and w by
means of a preliminary analysis in MARK, the
models that indicated different u and w
between males and females had only weak
support in the mark–recapture data compared
to models in which these parameters were set
as equal between sexes. These preliminary
results indicated that in S. grammicus growth
and survival rates do not differ between sexes,
at least in our study sites. Therefore, we
decided to use mark–recapture data for both
males and females to estimate stage- and site-
specific u and w with an increased sample
size. This pooled data set resulted in more-
precise parameter estimates. Therefore, in the
421
present study the permanence and growth
entries of our projection matrices were
calculated using data for both sexes.
The stage-specific probability of survival
with growth to a larger stage class (Gij) was
calculated as:
Gij ¼ uj 3 wij ;
where uj is the annual survival rate of
individuals in stage j and wij represents the
probability of transition from stage j to stage i.
The stage-specific probability of survival with
permanence in the same stage class (Pij, with
i ¼ j) was calculated as:
Pij ¼ uj 3ð1  wij Þ:
Stage-specific fecundity entries (Fij) repre-
sent the annual average number of juveniles
produced by an average reproductive female
from the corresponding adult category (Cas-
well, 2001). We used our estimates of annual
fecundity per reproductive stage class ob-
tained from captive females as fecundity
entries in our matrix models.
Estimating Population Growth Rates and the
Relative Importance of the Life-Cycle
Components
For each population we estimated the
annual rate of population increase (k) as the
dominant eigenvalue of each annual projec-
tion matrix (Caswell, 2001). We used elasticity
analysis to estimate the relative change in k
that would result from relative changes in
each matrix entry (de Kroon et al., 1986,
2000). Annual elasticity matrices (entries
denoted as eij) were constructed as:
eij ¼ sij 3ðaij =kÞ;
where sij represents the absolute sensitivity of
k to absolute changes in the matrix entries
(sij ¼ ]k/]aij; Caswell, 1978). As elasticities are
standardized sensitivities, they have been used
to compare the relative contribution of each
matrix entry to population growth rate (de
Kroon et al., 1986, 2000). In other words,
elasticities measure the relative importance of
the vital rates for average fitness (Benton and
Grant, 1999; Metcalf and Pavard, 2007).
Given that all entries in an elasticity matrix
sum to unity (Mesterton-Gibbons, 1993), we
422 HERPETOLOGICA
quantified the relative contribution of the life-
cycle components (i.e., permanence, growth,
and fecundity) to k simply by adding elasticity
values corresponding to each component (i.e.,
Silvertown et al., 1993). Specifically, the sum
of the elements in the main diagonal of an
elasticity matrix corresponds to the relative
importance of permanence for average fitness;
the sum of the elements in the subdiagonals
corresponds to the relative importance of
growth; and the sum of the elements in the
first row of an elasticity matrix corresponds to
the relative importance of fecundity.
Following Silvertown et al. (1993) we
plotted the elasticities for the three main
life-cycle components into the demographic
triangle, which is a three-way proportional
graph that provides a visual scheme to
compare the relative importance of perma-
nence, growth, and fecundity for average
fitness. Each axis in the triangle represents
the elasticity value of each life-cycle compo-
nent. To examine interpopulation variation in
the relative importance of these components,
we plotted one point for each study site.
Populations with a proportionately higher
elasticity value for one component (perma-
nence, growth, or fecundity) will be located
toward the corner of the triangle that corre-
sponds to the highest relative importance
(elasticity ¼ 1) of such component (Silvertown
et al., 1993).
Confidence intervals (95%) for k were
constructed using a resampling procedure.
MARK estimates survival (u) and growth (w)
rates from the regression coefficients (bi) of
complex linear models (Lebreton et al., 1992;
White and Burnham, 1999). We resampled
1000 new random values of these bi param-
eters based on normal distributions with the
mean equal to the point estimate of the
corresponding b and the standard deviation
equal to the standard error of the parameter
(also estimated by MARK). From these 1000
resampled estimates of bi we reconstituted
1000 new values of u and w for each
population and for each stage class. We also
resampled (bootstrapped) our reproductive
data to derive 1000 new average litter sizes
per stage and population. From these resam-
pled values of u, w, and litter size we
calculated 1000 new values for the matrix
[Vol. 69, No. 4
entries (Gij, Pij and Fij) and, from these, 1000
new k values. To construct the 95% confi-
dence intervals we used the 25th and 975th
sorted values of the resulting distribution of k
as the lower and upper limits, respectively.
Potential Associations between the Relative
Importance of the Life-cycle Components and
Environmental Factors
According to our predictions, we expected
high elasticity values for fecundity and growth
in those populations with mesic conditions
(i.e., with higher-than-average rainfall or
relatively large IR values), low population
density, and high microhabitat availability or
low degree of human disturbance (or a
combination of two or more of these condi-
tions). In addition, according to the fast–slow
continuum hypothesis, we expected increased
elasticity values for fecundity and growth in
populations with high mortality (i.e., low u).
In contrast, we expected high elasticity values
for permanence in those populations located
in more-arid areas (i.e., with higher-than-
average temperature or relatively low IR
values), high population density, and low
microhabitat availability or high degree of
human-induced disturbance (or a combina-
tion of two or more of these conditions).
According to the fast–slow continuum hypoth-
esis, increased relative importance of perma-
nence is expected in low-mortality
environments (i.e., high u). We tested for
statistical relationships between the relative
importance of the life-cycle components and
the site-specific aridity indexes, residual val-
ues of rainfall and temperature, estimates of
population density, and estimates of overall
mortality (calculated as an average mortality
rate across stage classes). We also tested for
differences in the relative importance of the
life-cycle components between sites with low
and high microhabitat availability and among
wild areas, agriculture lands, and urban areas.
However, given that elasticity values for
permanence, growth, and fecundity are highly
dependent on each other (e.g., increasing the
elasticity for permanence necessarily implies
decreasing elasticities for either growth or
fecundity), we calculated a combined measure
of the relative importance of these life-cycle
components. For this purpose we conducted a
December 2013] HERPETOLOGICA
principal components analysis (PCA) on these
elasticity values. Only the first principal
component had an eigenvalue . 1. We used
the site-specific scores in this main axis of
variation as a combined estimate of the
relative importance of permanence, growth,
and fecundity. We used pairwise Spearman
Correlation coefficients to test for potential
associations between this combined measure
and our site-specific IR values, residual values
of rainfall and temperature, estimates of
population density, and overall mortality rates.
We also compared site-specific scores in this
first principal component between sites with
low and high microhabitat availability and
among wild areas, agriculture lands, and
urban areas by means of a Mann–Whitney
U-test and a Kruskal–Wallis test, respectively.
All the environmental factors that we
studied could have interacted to determine
the relative importance of the life-cycle
components for the average fitness of S.
grammicus. Therefore, we constructed linear
models to test for statistical effects of two-way
interactions between residual rainfall, residual
temperature, aridity, population density, mi-
crohabitat availability, and extrinsic mortality
on the site-specific scores in the first principal
component. We did not test for interactions
among three or more environmental factors
because of our lack of degrees of freedom.
Similarly, we did not test for interactions
between degree of human-induced distur-
bance and any other variable because we
had only two sites in the category ‘‘wild
areas.’’
RESULTS
Model Selection
In four out of the eight studied populations,
the best-fitting model indicated that u was
similar across time and stage classes and was
not affected by population density (i.e.,
constant u in Sites 1, 3, 5, and 7). In three
other populations the best-fitting model indi-
cated a density-dependent u (in Sites 2, 6, and
8). In the remaining population the best
model indicated that u varied among stage
classes (in Site 4; Table 3). However, in five
out of our eight sites there was uncertainty
with respect to the actual sources of variation
423
for u (i.e., in Sites 3, 5, 6, 7, and 8 other
models had DAICc , 2). A density-dependent
effect on u also had good fit and considerable
support in the data of Sites 3, 5, and 7
(DAICc , 2; Table 3). An effect of stage class
on u also had good fit and considerable
support in the data of Sites 6 and 8.
Occasion-specific differences in u (i.e., time-
dependency) were not supported by our
mark–recapture data on any study site.
Regarding sources of variation for p, in five
populations the best-fitting model indicated
that this parameter varied mainly among stage
classes (in Sites 2, 3, 6, 7, and 8). In two other
populations (Sites 1 and 5) the best-fitting
model indicated p was constant across time
and stage classes and was not affected by
population density. In the remaining popula-
tion p varied among capture occasions (in Site
4; Table 3). In four study sites we found
uncertainty with respect to the actual sources
of variation for p (in Sites 3, 5, 7, and 8 other
sources of variation for p had DAICc , 2;
Table 3).
Regarding sources of variation for w, an
effect of stage class had the strongest support
in five out of our eight study sites (in Sites 1, 3,
4, 5, and 8). In four of these sites, there was no
uncertainty in the fact that w varied among
stage classes (i.e., in Sites 1, 3, 4, and 5, only
models with a stage-class effect on w had good
fit to the data; Table 3). In another site (Site 7)
this stage-class effect also had support com-
parable to that of the best-fitting model
(DAICc , 2). Time-dependent w had the best
fit to our data in Site 2, density-dependent w
had the best fit in Site 6, and constant w had
the best fit in Site 7. Uncertainty in the actual
sources of variation for w occurred in Sites 7
and 8 only (Table 3).
Stage-specific Vital Rates
Annual stage-specific survival rates (u)
varied widely: between 0.14 (for juveniles of
Site 4) and 0.65 (for juveniles of Site 1; Table
4). Two study populations resulted in notably
high u values for most stage classes (above 0.5
in Sites 1 and 6). One of these populations
(Site 1) corresponded to the most-arid site
(IR ¼ 1398.12) whereas the other one (Site 6)
corresponded to a relatively humid site (IR ¼
2704.15; Table 1). In five study sites annual u
424 HERPETOLOGICA
was similar among stage classes (in Sites 1, 2,
3, 5, and 7). In the remaining three popula-
tions annual u varied markedly among stage
classes (in Sites 4, 6, and 8; Table 4).
Annual transition between stage classes (w)
also exhibited great variation among popula-
tions and stage classes (Table 4). Differences
among stage classes in the magnitude of this
parameter represented a clear pattern of
variation because in most sites w was highest
for the transition from juveniles to small
adults (Table 4). This result indicates that,
within populations, the largest rates of body
growth occurred in juveniles. Nevertheless,
we found wide variation among populations in
this transition rate between juveniles and
small adults. In four sites this parameter was
markedly low (between 0.04 and 0.09 in Sites
2, 6, 7, and 8) whereas in one site this annual
parameter was markedly high (0.78 in Site 1).
This highest w value occurred in the most-arid
site (IR ¼ 1398.12; Table 1). In contrast,
transition from small to large adults varied
between 0.04 and 0.11 among populations.
The lowest w values corresponded to the
transition from juveniles to large adults. These
low w values resulted from the few fast-
growing juveniles that reached a large adult
size within a single year. This transition rate
between juveniles and large adults also varied
widely among populations: between less than
0.001 (in Site 5) to 0.06 (in Site 6; Table 4).
Annual fecundity rates exhibited less varia-
tion among populations and stage classes
(Table 4). In six out of our eight study sites
the average number of offspring produced per
female was equal between small and large
adults. Only in Sites 2 and 4 did fecundity
differ between stage classes, with large adults
having higher fecundity than small adults
(Table 4). However, the number of pregnant
females that we had with which to estimate
fecundity was low in most populations (Table
4). Therefore, we lacked statistical power to
detect differences among populations or
between stage classes. The lowest fecundity
value observed among populations was 2.57
newborns in small females of Site 2. The
highest fecundity value observed among
populations was 6.67 newborns in large
females of Site 4 (Table 4). Average litter size
[Vol. 69, No. 4
among populations and stage classes was 3.94
offspring per female.
Potential Associations between Vital Rates and
Environmental Factors
Site-specific values of residual rainfall,
residual temperature, and aridity (IR) were
not significantly related to stage-specific esti-
mates of u, w, or fecundity (P . 0.05 in all
cases). Similarly, we found no statistical
differences between low and high microhab-
itat availability or among wild areas, agricul-
ture lands, and urban areas in stage-specific u,
w, or fecundity (P . 0.05 in all cases). With
respect to population density (site-specific
estimates of population density are shown in
Table 1), only fecundity of small adults
exhibited a significant relationship with den-
sity (rS ¼ 0.74, P ¼ 0.03). This relationship was
positive, meaning that sites with a greater
density of lizards were related to a greater
number of offspring produced by small adult
females. No other significant relationships
between stage-specific u, w, or fecundity and
site-specific population density were found
(P . 0.05 in all other cases).
We found a significant interaction between
IR and microhabitat availability affecting the
survival of small adults (F3,4 ¼ 19.47, P ¼
0.008). In sites with low microhabitat avail-
ability, u of small adults decreased as IR
increased (i.e., under less-arid conditions; Fig.
2A). In contrast, in sites with high microhab-
itat availability, u of small adults appeared to
increase as IR increased (Fig. 2A). We also
found a significant interaction between pop-
ulation density and microhabitat availability
affecting the survival of large adults (F3,4 ¼
8.03, P ¼ 0.04). In sites with low microhabitat
availability, u of large adults decreased as
population density increased (Fig. 2B). In
contrast, in sites with high microhabitat
availability there was no effect of population
density on u of large adults (Fig. 2B). No
other interaction between environmental fac-
tors affecting stage-specific u, w, or fecundity
was statistically significant.
Population Growth Rates and the Relative
Importance of the Life-cycle Components
Five out of our eight populations had a
finite rate of increase (k) that was not
December 2013] HERPETOLOGICA 425

FIG. 2.—(A) Relationship between site-specific aridity (measured by means of the Reichel’s aridity index) and the
survival of small adults for sites with low (continuous line) and high (dashed line) microhabitat availability. (B)
Relationship between site-specific population density and the survival of large adults for sites with low (continuous line)
and high (dashed line) microhabitat availability. Survival estimates were arcsine transformed. Numbers indicate sites as
per Table 1.
426 HERPETOLOGICA [Vol. 69, No. 4

TABLE 5.—Population projection matrices, finite rates of population growth (k), and elasticity matrices for eight
populations of the viviparous lizard Sceloporus grammicus. The k values in bold type indicate population growth rates
significantly different from unity. Elasticity values in bold type correspond to the largest elasticities for each population.

Population projection matrix Elasticity matrix

a b c
Site J SA LA k J SA LA

1 J 0.2 3.33 3.33 1.69 (1.09–1.89) 0.03 .369 0.03

SA 0.51 0.51 0 0.37 0.16 0
LA 0.02 0.5 59 0.01 0.02 0.02
2 J 0.22 2.57 4.14 0.49 (0.08–1.75) 0.21 0.11 0.15
SA 0.01 0.25 0 0.11 0.12 0
LA 0.01 0.01 .25 0.14 7.0E-03 0.16
3 J 0.13 3.5 3.5 0.63 (0.43–1.08) 0.10 0.36 0.01
SA 0.06 0.18 0 0.37 0.15 0
LA 4.2 E-04 0.01 0.19 2.5 E-03 6.5 E-03 3.9 E-03
4 J 0.09 4 6.67 0.78 (0.61–1.05) 0.04 0.23 0.05
SA 0.05 .44 0 0.27 0.34 0
LA 9.1 E-04 0.05 0.29 4.9 E-03 0.04 0.03
5 J 0.12 4.34 4.34 0.83 (0.73–1.01) 0.07 0.38 0.01
SA 0.10 0.20 0 0.39 0.12 0
LA 2.8 E-07 0.02 0.22 1.1 E-06 0.01 5.4 E-03
6 J 0.44 3.94 3.94 0.97 (0.43–1.76) 0.22 0.11 0.15
SA 0.04 0.25 0 0.12 0.04 0
LA 0.03 0.02 0.54 0.15 4.6 E-03 0.20
7 J 0.14 3.5 3.5 0.42 (0.41–0.81) 0.15 0.20 0.11
SA 0.01 0.17 0 0.21 0.14 0
LA 6.7 E-03 0.01 0.17 0.10 0.01 0.08
8 J 0.22 4.2 4.2 0.63 (0.50–0.92) 0.13 0.18 0.06
SA 0.02 0.38 0 0.19 0.31 0
LA 6.8 E-03 0.02 0.30 0.05 0.01 0.06
a
Numbers were assigned to sites according to the aridity index: from low to high IR values (from more to less arid). These numbers identify sites throughout
the text.
b
J ¼ juveniles; SA ¼ small adults; LA ¼ large adults.
c
Confidence intervals (95%) for k are shown within parentheses.

significantly different than unity, indicating Among populations, the relative importance
population stability (Sites 2, 3, 4, 5, and 6; of permanence varied between 0.20 (in Site 5)
Table 5). In contrast, one population had a k and 0.50 (in Site 8). The relative importance
value that was significantly above unity, of growth varied between 0.26 (in Site 8) and
indicating potential for population growth 0.41 (in Site 5). The relative importance of
(k ¼ 1.69 in Site 1). This highest k value fecundity varied between 0.25 (in Site 8) and
corresponded to the most-arid site (IR ¼ 0.39 (in Site 5; Table 6). In general, all
1398.12). The remaining two populations populations were located in the central
resulted in k values that were significantly
below unity, indicating potential for popula- TABLE 6.—Elasticity values for the three components of
tion decrease (k ¼ 0.42 in Site 7 and k ¼ 0.63 the life cycle for eight populations of the viviparous lizard
Sceloporus grammicus.
in Site 8; Table 5). These lowest k values
corresponded to the least-arid sites (IR ¼ Sitea Permanence Growth Fecundity
2802.53 in Site 7 and IR ¼ 3251.24 in Site 8). 1 0.21 0.40 0.39
Populations varied widely in terms of the 2 0.48 0.26 0.26
vital rates with highest elasticities (Table 5). In 3 0.25 0.38 0.37
4 0.41 0.32 0.28
general, the highest elasticity values corre- 5 0.20 0.41 0.39
sponded to growth and permanence of 6 0.46 0.27 0.27
juveniles as well as to fecundity and perma- 7 0.37 0.32 0.31
nence of small adults. Fecundity and perma- 8 0.50 0.26 0.25
a
nence of large adults had relatively low Numbers were assigned to sites according to the aridity index: from low
to high IR values (from more to less arid). These numbers identify sites
elasticities in all sites (Table 5). throughout the text.
December 2013] HERPETOLOGICA 427

FIG. 3.—Ordination of the eight study populations of the viviparous lizard Sceloporus grammicus within the
demographic triangle according to the relative contribution of the life-cycle components to the finite rate of population
growth. Numbers indicate sites as per Table 1. Colors indicate degree of human-induced disturbance: white ¼ wild
areas, grey ¼ agriculture lands, black ¼ urban areas.

portion of the demographic triangle, indicat-
ing that all three life-cycle components had
relatively similar elasticity values. However, a
continuum of variation in the relative impor-
tance of these life-cycle components was
evident, from populations with higher impor-
tance of growth and fecundity (i.e., Sites 1, 3,
and 5; Fig. 3) to populations with higher
importance of permanence (i.e., Sites 2, 6, and
8; Fig. 3).
Potential Associations between the Relative
Importance of the Life-cycle Components and
Environmental Factors
The first principal component that summa-
rized the site-specific relative importance of
the life-cycle components for population
growth rate resulted in the following loadings:
permanence ¼ 1.00, growth ¼ 0.99, and
fecundity 0.99. The signs of these loadings
indicate that populations with high scores in
this axis had relatively higher elasticity for
permanence and relatively lower elasticities
for growth and fecundity. In contrast, popu-
lations with low scores in this axis had
relatively higher elasticities for growth and
fecundity and relatively lower elasticity for
permanence. The site-specific scores in this
first principal component were not statistically
associated with site-specific population densi-
ty, residual temperature, residual rainfall,
aridity, or overall mortality (P . 0.05 in all
cases). Interpopulation differences in micro-
habitat availability and degree of human-
induced disturbance could not explain the
observed interpopulation variation in the
relative importance of the life-cycle compo-
nents (U ¼ 7.0, P ¼ 0.77 and H ¼ 2.25, P ¼
0.32, respectively). The two-way interactions
between these environmental factors did not
significantly affect the site-specific scores in
this principal component either (P . 0.05 in
all cases). In other words, the relative position
of the study populations within the demo-
graphic triangle could not be explained by
interpopulation differences in the environ-
mental characteristics that we studied or by
their interactions (Fig. 3).
428 HERPETOLOGICA
DISCUSSION
Intraspecific Variation in Stage-specific
Vital Rates
Stage-specific survival and transition rates
were highly variable among sites, suggesting
that different ecological and evolutionary
processes are currently taking place in our
eight studied populations (Oriazola and Laur-
ila, 2009; Miller et al., 2011). High interpop-
ulation variation in survival has been
documented in several species of quite diverse
taxa (e.g., Miller et al., 2011; Papadatou et al.,
2011; Welch et al., 2011; Wilson and Martin,
2011), including lizards (Jessop et al., 2007;
Iraeta et al., 2008; Rojas-González et al.,
2008). Annual survival in S. grammicus can
be as low as 14% and as high as 65%
depending on the source population (Table
4). The highest survival rates were observed in
Site 1 (between 56% and 65%), which
corresponds to the most-arid conditions (Ta-
ble 1). This result is opposite to what we
expected: highest survival rates in sites with
higher water availability and milder tempera-
tures.
Transition rates between stage classes were
highest for juveniles growing to small adults.
This pattern occurred in most populations and
was well supported by our mark–recapture
data (Table 4). In vertebrates, young and small
individuals usually exhibit the fastest rates of
body growth (Dunham, 1978; Andrews, 1982;
Arendt, 1997; Zúñiga-Vega et al., 2005, 2008b;
Dibattista et al., 2007). Besides this clear
difference among stage classes in transition
rates, significant variation also occurred
among populations. The percentage of surviv-
ing juveniles that progressed to small adults
varied from 4% in Site 2 to 78% in Site 1 (an
almost 20-fold difference). Moreover, the
percentage of surviving juveniles that grew
even faster, progressing to large adults within
a single year, varied from less than 0.1% in
Site 5 to 6% in Site 6 (a 60-fold difference).
Annual transition between small and large
adults was less variable, ranging only from 4%
in Sites 2 and 3 to 11% in Sites 4 and 5.
Similar to our findings in survival rates, the
highest transition rate (78% of surviving
juveniles progressing to small adults within a
year) occurred at the most-arid site (Site 1).
[Vol. 69, No. 4
Fecundity rates were less variable com-
pared to survival or transition rates. The
observed range of variation among popula-
tions was between 2.57 and 6.67 young per
female (a 2.6-fold difference). Moreover, in six
out of our eight study sites the average
number of offspring produced per female
was similar between small and large adults.
This finding contrasts with previous studies on
S. grammicus that have demonstrated that
female size exhibits a significant positive
relationship with litter size (Guillette and
Casas-Andreu, 1980; Ortega-Rubio and Bar-
bault, 1984; Guillette and Bearce, 1986;
Lemos-Espinal et al., 1998; Ramı́rez-Bautista
et al., 2004). The lack of a size effect on
fecundity, which we observed in six popula-
tions, might be simply the result of our small
sample sizes (Table 4).
Potential Effects of Environmental Factors on
Stage-specific Vital Rates
No statistical relationships were observed
between vital rates and aridity, residual
rainfall, or residual temperature. Several
authors have demonstrated that rainfall and
temperature are key determinant factors of
the life-history traits of ectotherms (Sinervo et
al., 2010; Arendt, 2011). Hence, we expected
relatively slow body growth, low survival, or
decreased fecundity (or any combination) in
populations inhabiting the warmest and driest
environments or during years with higher-
than-average temperature, lower-than-aver-
age rainfall, or both. Our results do not
support these predictions. In contrast, we
found some evidence for the opposite pattern
in S. grammicus: the highest survival and
transition rates (between juveniles and small
adults) occurred in the most-arid site (Site 1;
IR ¼ 1398.12). However, in the second-most
arid site (Site 2; IR ¼ 1438.86), relatively low
survival and transition rates were observed
(Table 4). Therefore, neither aridity condi-
tions nor the particular levels of temperature
or rainfall that these lizards experienced
during our study period could explain the
observed interpopulation variation in stage-
specific survival, growth, and fecundity.
Fecundity of small adults increased in sites
with a high density of lizards. This finding is
opposite to what we expected based on the
December 2013] HERPETOLOGICA
widely observed negative effects of density on
the vital rates of vertebrates: decreased
survival, growth, and fecundity in high-density
conditions (Calsbeek and Smith, 2007; Einum
et al., 2008; Mappes et al., 2008; Manteuffel
and Eiblmaier, 2010). In contrast, this positive
relationship between small adult fecundity
and density suggests positive density-depen-
dence (e.g., Ferrer and Penteriani, 2008;
Ashbrook et al., 2010; Belk and Tuckfield,
2011). At this point the causes of this apparent
positive effect of density remain unknown.
One possibility is that sites with a high density
of lizards (i.e., Sites 5, 7, and 8; Table 1) might
correspond to markedly favorable conditions
(for instance in terms of food availability),
which might also allow for increased fecundi-
ty. Alternatively, this statistical relationship
between the number of young produced by
small adults and population density might be
spurious.
We also predicted effects of both micro-
habitat availability and degree of human-
induced disturbance on the vital rates of S.
grammicus. Specifically, we expected low
survival, growth, or fecundity (or all) in sites
with a low number of potential refuges or sites
for perching, or in sites with high disturbance
such as urban areas. Human-induced distur-
bance was not related to interpopulation
variation in vital rates. In contrast, microhab-
itat availability had an effect on the survival of
small and large adults. However, microhabitat
availability could not explain, by itself, some of
the variation that we observed in survival
rates. Microhabitat availability had an inter-
active effect with site-specific aridity and
population density on the survival of small
and large adults, respectively (Fig. 2). In less-
arid conditions, survival of small adults
decreased in sites with low microhabitat
availability but not in sites with high micro-
habitat availability. This result indicates that
mesic sites, which usually have more cloudy
days as a result of increased rainfall, might
entail thermal restrictions with severe effects
for small adults. However, these negative
effects are evident only in sites with low
microhabitat availability. In turn, under high-
density conditions survival of large adults
decreased in sites with low microhabitat
availability but not in sites with high micro-
429
habitat availability. Therefore, the potential
negative effects of adverse environmental
conditions are stronger (i.e., detectable) only
in populations that experience constraints in
perch sites or refuges. This finding indicates
that environmental factors act in conjunction
to shape the demographic traits of S. gram-
micus.
Population Growth Rates and the Relative
Contribution of the Life-cycle Components to
Average Fitness
Finite rates of population growth (k)
indicated demographic stability in five out of
our eight studied sites. Two other populations
(Sites 7 and 8) resulted in k values that
suggested population declines. These two
populations corresponded to the sites with
the least-arid conditions (highest water avail-
ability; Table 1), which is contrary to what we
expected. However, these two sites are urban
areas with a high degree of human-induced
disturbance and, in addition, population
density of these lizards is relatively high in
both sites (Tables 1 and 2). These two
negative factors combined might explain the
observed low population growth rates in Sites
7 and 8. Alternatively, low population growth
rates could be expected in years with higher-
than-average temperature or lower-than-aver-
age rainfall (or both). This was not the case for
Sites 7 and 8 in our studied years. In fact,
2009, 2010, and 2011 in Site 8 were slightly
colder years than the historical interannual
trend. With respect to rainfall, in Site 7 the
total amount of rainfall during our studied
years was similar to that expected based on
the past interannual trend. In Site 8, the
amount of rainfall during our studied years
was quite similar to the historical average. The
remaining population (Site 1) resulted in a k
value that indicates significant potential for
population increase. The highest survival rates
observed among populations occurred in this
site as well as a strikingly high progression rate
between juveniles and small adults (0.78;
Table 4). This population is located in the
most-arid site (Table 1), which again is
contrary to what we expected. However, it is
an undisturbed area with the lowest popula-
tion density (Tables 1 and 2). Additionally, the
highest historical average temperature oc-
430 HERPETOLOGICA
curred at this site (Table 1), and 2009 and
2011 were years with higher than average
environmental temperature. Contrary to what
we expected for S. grammicus, relatively high
temperatures might improve physiological
performance, body growth, and survival
chances if thermoregulating activities are
effective enough to offset the costs of low
water availability (Grant, 1990; Sinervo and
Adolph, 1994; Angilleta, 2009). In contrast,
less-arid sites with lower temperatures and
more rainy days could entail thermal restric-
tions that would result in reduced physiolog-
ical performance and lower rates of body
growth. A line of evidence that supports this
hypothesis is the fact that in the least-arid sites
(Sites 6, 7, and 8; Table 1) stage-specific
transition rates were notably low (Table 4).
Therefore, the interactive effects of thermal
restrictions, high population densities, and
human-induced disturbance likely caused the
lowest rates of population growth that we
detected in Sites 7 and 8.
We recognize that natural populations
experience periods of population growth and
periods of population decline. In the long
term, the combination of these contrasting
trends results in demographic stability (e.g.,
Webb et al., 2002; Iverson et al., 2006;
Zúñiga-Vega et al., 2007). For those popula-
tions in which we observed finite rates of
population growth significantly lower (Sites 7
and 8) or higher (Site 1) than unity, our
studied years might have coincided with short-
term unfavorable or favorable conditions,
respectively. Based on our data set, which
spans a little over 2 yr (July 2009–November
2011), we cannot extrapolate that the ob-
served declines (in the case of Sites 7 and 8)
will lead to extirpation or that the observed
population growth (in the case of Site 1) will
lead to a considerable increase in the density
of these lizards.
The relative importance of the three life-
cycle components (permanence, growth, and
fecundity) for average fitness was relatively
similar. In other words, no single component
had a strikingly high elasticity value such as
has been observed in other organisms. For
example, long-lived species such as turtles or
trees are usually associated with permanence,
explaining more than 90% of the observed k
[Vol. 69, No. 4
values (i.e., elasticity for permanence . 0.9;
Heppell, 1998; Franco and Silvertown, 2004;
Macip-Rı́os et al., 2011). Ruderal plants or
short-lived mammals usually show an opposite
trend: fecundity is the process making a
remarkably high contribution to fitness com-
pared to growth or permanence (Heppell et
al., 2000, Franco and Silvertown, 2004). In S.
grammicus all three processes had elasticity
values . 0.19, and this can be graphically
observed in the central position of the studied
populations within the demographic triangle
(Fig. 3). However, some variation was ob-
served and we expected that the relative
importance of the three life-cycle components
was related to residual temperature, residual
rainfall, aridity, population density, microhab-
itat availability, degree of human-induced
disturbance, or extrinsic mortality.
Potential Effects of Environmental Factors on
the Relative Importance of the Life-cycle
Components for Average Fitness
None of the environmental factors that we
studied was statistically associated with inter-
population variation in the elasticities for
permanence, growth, or fecundity. Interac-
tions between such factors did not affect the
relative importance of the life-cycle compo-
nents either. Contrary to our predictions, this
lack of associations indicates that these factors
are not determinants for how these organisms
allocate resources to each of these processes.
We detected some effects of population
density on fecundity as well as some effects
of the interactions of microhabitat availability
with aridity and with density on survival, but
these effects did not translate into relation-
ships between these factors and the observed
elasticity patterns. In addition, our elasticity
analysis revealed that the small stage classes
(juveniles and small adults) made the greatest
contribution to fitness in all populations,
regardless of the large differences among sites
in environmental conditions and in the stage-
specific vital rates. An alternative explanation
to the observed interpopulation variation in
the relative importance of the life-cycle
components for average fitness focuses on
historical processes rather than on environ-
mentally driven factors. As we recognized
before, our populations might belong to
December 2013] HERPETOLOGICA
distinct chromosomal races (Arévalo et al.,
1994). Therefore, similar chromosomal races
might share similar survival, growth, or
fecundity rates (or all) and, in turn, similar
elasticity patterns just because of shared
ancestry. Accurate descriptions of the chro-
mosomal races at our study sites and the
phylogeographic history of these populations
are needed to test this hypothesis.
The fast–slow continuum of life-history
evolution suggests that species or populations
experiencing high extrinsic mortality will
evolve ‘‘fast’’ life cycles with increased body
growth and fecundity. This, in turn, would
result in fecundity and growth making the
largest contributions to average fitness. In
turn, populations experiencing low extrinsic
mortality will evolve ‘‘slow’’ life cycles with
delayed body growth and reduced fecundity.
This, in turn, would result in a significantly
larger contribution of permanence to average
fitness compared to modest contributions of
growth and fecundity (Promislow and Harvey,
1990; Franco and Silvertown, 1996; Oli, 2004).
This hypothesis was not supported by our
results. More important, this lack of associa-
tion between mortality and the relative
importance of the life-cycle components is
not consistent with what has been observed in
other systems. In several species of plants
(Franco and Silvertown, 1996), birds (Sæther
and Bakke, 2000), and mammals (Heppell et
al., 2000; Oli and Dobson, 2003), extrinsic
mortality explains a large proportion of the
interspecific variation in the relative contribu-
tion of permanence, growth, and fecundity to
fitness. However, these patterns of variation
and association have been examined among
species. The present study is one of the few
examining the demographic predictions of the
fast–slow continuum hypothesis within a
single species (Horvitz and Schemske, 1995;
Silvertown et al., 1996; Floyd and Ranker,
1998; Heppell, 1998) and certainly the first
focused on a lizard species. Perhaps differ-
ences in mortality rates among populations of
single species must remain constant through
long periods of time in order to promote the
expected differences in the relative impor-
tance of the life-cycle components for average
fitness. However, within populations, tempo-
ral variation in mortality and in other vital
431
rates may be as high as that observed among
populations. Thus, a complete picture of the
long-term effects of extrinsic mortality on
intraspecific variation in life-history traits will
be achieved only by studying several popula-
tions during long periods of time (more than
10 yr; Crone et al., 2011).
Finally, within-year variation in the relative
importance of the life-cycle components for
average fitness likely occurs in our studied
populations. In species inhabiting arid or
semi-arid environments, such as S. grammi-
cus, the time periods that are benign for
growth and reproduction are short and
sometimes unpredictable. In these cases,
natural selection promotes the evolution of
plastic responses such as increased reproduc-
tive effort or body growth during such periods
(Venable, 2007). Therefore, drastic changes in
the relative importance of the life-cycle
components for average fitness can be expect-
ed within single years, such as higher elastic-
ities for growth and fecundity during favorable
periods and higher elasticity for permanence
during the rest of the year. Such expected
short-term changes in the relative importance
of the life-cycle components for average
fitness and their underlying environmental
causes deserve future research.
Acknowledgments.—This paper is a requisite to obtain
the Ph.D. degree in the Posgrado en Ciencias Biológicas
of Universidad Nacional Autónoma de México. We would
like to thank the Consejo Nacional de Ciencia y
Tecnologı́a 210458 and the Programa de Apoyo a
Proyectos de Investigación e Innovación Tecnológica
(project PAPIIT-IN206309-3) from Universidad Nacional
Autónoma de México for the financial support provided
for this research. Also we would like to thank C. Martorell
for his comments, which improved this study. Finally, we
thank P. Mendoza-Hernández, J. Maceda-Cruz, L.
Moyers-Arévalo, M. Romano-Garcı́a, C. Molina-Zuluaga,
C. Olivera-Tlahuel, and F. Rodrı́guez-Reyes for field
assistance. Fieldwork was conducted under permit
FAUT-0240 issued by the Dirección General de Vida
Silvestre – México.
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Accepted: 8 August 2013
Associate Editor: Stephen Mullin