Vegetation Cover and Road Density as Indicators of Habitat Suitability for the

Morelet's Crocodile
Author(s): Ricardo González-Trujillo, Rodrigo Méndez-Alonzo, Víctor Arroyo-Rodríguez, Ernesto Vega,
Alberto González-Romero, and Víctor H. Reynoso
Source: Journal of Herpetology, 48(2):188-194. 2014.
Published By: The Society for the Study of Amphibians and Reptiles
DOI: http://dx.doi.org/10.1670/12-150
URL: http://www.bioone.org/doi/full/10.1670/12-150

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Journal of Herpetology, Vol. 48, No. 2, 188–194, 2014
Copyright 2014 Society for the Study of Amphibians and Reptiles

Vegetation Cover and Road Density as Indicators of Habitat Suitability

for the Morelet’s Crocodile

RICARDO GONZÁLEZ-TRUJILLO,1,2,3 RODRIGO MÉNDEZ-ALONZO,4 VÍCTOR ARROYO-RODRÍGUEZ,5 ERNESTO VEGA,5

ALBERTO GONZÁLEZ-ROMERO,1 AND VÍCTOR H. REYNOSO2
1
Red de Biologı́a y Conservación de Vertebrados, Instituto de Ecologı́a A.C. Xalapa, Veracruz 91070, Mexico
2
Departamento de Zoologı́a, Instituto de Biologı́a, Universidad Nacional Autónoma de México, Mexico city 04510, Mexico
4
Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California 90095 USA
5
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México Morelia, Michoacán 58190, Mexico

ABSTRACT.—Understanding the response of species to land-use change is necessary for the improvement of management and conservation
policies. We assessed the impact of vegetation cover and land-use change on Morelet’s crocodile populations in nine wetlands located in central
Veracruz, Mexico, to test the hypothesis that higher forest cover and lower anthropogenic impact increases crocodile density. We correlated the
relative density of crocodiles with wetland attributes, including depth, pH, salinity, and richness and structure of bordering vegetation; and
with anthropogenic disturbance factors, including the proportion of modified land surrounding the water body, road density, and road type. The
relative density of crocodiles was correlated positively with vegetation cover and correlated negatively with plant density and with the presence
of nonpaved roads, particularly in the zone that bordered the water bodies (core zone). Our findings suggest that as long as the water bodies are
bordered with arboreal vegetation, land-use change and paved road density in inland areas had minor impacts on Morelet’s crocodile
populations in Mexican wetlands. The vegetation cover and the number of nonpaved roads within the core zone are useful indicators of habitat
suitability for the Morelet’s crocodile. The conservation of mangroves and forest remnants is therefore essential for the maintenance of
crocodile populations.

RESUMEN.—Entender la respuesta de las especies al cambio de uso del suelo es necesario para mejorar las polı́ticas de gestión y conservación de
los recursos naturales. Evaluamos el impacto de la cobertura vegetal y el cambio de uso del suelo sobre nueve poblaciones del cocodrilo de
pantano localizadas en el centro de Veracruz, México. Se sometió a prueba la hipótesis de que el aumento en la cobertura forestal y la reducción
del impacto antrópico incrementan la densidad de cocodrilos. Correlacionamos las densidades relativas de los cocodrilos con atributos de los
humedales, tales como profundidad, pH, salinidad, riqueza y estructura de la vegetación, y con atributos de disturbio antropogénicos como la
proporción de tierras modificadas que rodean el cuerpo de agua, la densidad de caminos y los tipos de carretera. La densidad relativa de los
cocodrilos aumentó cuando la proporción de cobertura vegetal natural fue mayor y disminuyó con la el aumento en el número de carreteras no
pavimentadas, particularmente cuando éstas se encontraban alrededor de los cuerpos de agua (zona núcleo). Nuestros hallazgos sugieren que,
mientras que los cuerpos de agua estén rodeados de vegetación arbórea, el cambio de uso de suelo y la densidad de carreteras pavimentadas
lejanos al cuerpo de agua tendrán un impacto mı́nimo sobre las poblaciones de cocodrilo de pantano en los humedales mexicanos. La cobertura
de la vegetación en la zona núcleo y el número de carreteras no pavimentadas son indicadores útiles de calidad del hábitat para el cocodrilo de
pantano. La preservación de los bosques remanentes y los manglares es esencial para el mantenimiento de las poblaciones de cocodrilos.

The global decline of many plant and animal populations is
caused mainly by the accelerated and extensive anthropogenic
modification of terrestrial ecosystems (Meyer and Turner, 1992;
Lambin et al., 2003; Turner et al., 2007); however, the
information available for inland aquatic ecosystems (e.g.,
streams, rivers, floodplains, lakes, and swamps) is very scarce.
Inland aquatic ecosystems are also strongly affected by land-use
practices and other human activities (FAO, 2012). In fact,
because of the wide range of ecosystem services that aquatic
ecosystems provide, human settlements are commonly located
near inland water bodies and alter the species that inhabit these
ecosystems (Cohen et al., 1997; Costanza et al., 1997; Sala et al.,
2000; FAO, 2012). Because inland water bodies provide habitats
for many aquatic and semiaquatic species, conservation efforts
may be misguided unless the main threats to species persistence
in these ecosystems can be identified (Sullivan and Sullivan,
2006).
There is increasing evidence that semiaquatic species, such as
amphibians and reptiles, are particularly vulnerable to alter-
ations in the vegetation cover along the borders of water bodies.
For example, the density and richness of salamander and reptile
species decreases when the wetland vegetation cover is
modified (Findlay and Houlahan, 1997; Willson and Dorcas,
3
Corresponding author. E-mail: ricarcass@gmail.com
DOI: 10.1670/12-150
2003). Crocodilians prefer nesting in sites with dense vegetation
along the borders of shorelines; hence, nest density can be lower
when arboreal vegetation is modified or eliminated (Groom-
bridge, 1987; Stafford et al., 2003; Cedeño-Vázquez et al., 2006).
However, despite the vulnerability of semiaquatic species to
anthropogenic influence, information on the topic remains
scarce.
Another source of anthropogenic impact on wetlands is road
construction. Killings caused by collisions are considered to be
among the major causes of animal death in human-dominated
landscapes, particularly for slow-moving terrestrial or semi-
aquatic animals such as amphibians, tortoises, and crocodilians
(Forman and Deblinger, 2000; Trombulak and Frissell, 2000;
Carr and Fahrig, 2001; Gibbs and Shriver, 2002; Fahrig and
Rytwinski, 2009; Rytwinski and Fahrig, 2012). The construction
of roads close to water bodies imposes limits on the dispersal
and movement of semiaquatic vertebrates, increasing their
probability of local extirpation (Findlay and Bourdages, 2000).
For example, the construction of roads impacts crocodiles by
reducing the establishment and connectivity of populations
(Fennessy et al., 2004). Therefore, it is necessary to combine local
(e.g., vegetation surveys) and landscape-scale evaluations (e.g.,
land cover and road-density studies) to evaluate habitat
suitability accurately for semiaquatic species (Burke and
Gibbons, 1995; Semlitsch and Jensen, 2001; Schabetsberger et
al., 2004; Aust, 2009).
 HABITAT SUITABILITY FOR CROCODYLUS MORELETII
FIG. 1. Study sites in central Veracruz, Mexico: Ciénegas del Fuerte
Popal (CFP), Ciénegas del Fuerte Selva (CFS), Estero Dulce (ED), Casitas
(CS), Laguna Chica (LC), La Mancha (LM), San Julián (SJ), Rı́o Caña
(RC), and Popotera (PO). The hatching within the inset depicts the
natural range of C. moreletii.
The Morelet’s crocodile (Crocodylus moreletii, Dumeril and
Bibron, 1851) represents a valuable model species for the
assessment of the impact of habitat alteration on semiaquatic
species in inland water bodies. This species is relatively easy to
survey, and similar to other crocodiles, it is expected to be
highly vulnerable to threatening anthropogenic activities
(Kushlan, 1988; Trombulak and Frissell, 2000). Crocodiles are
also top predators, and their elimination can alter the balance of
food webs in freshwater and estuarine ecosystems (Mazzotti et
al., 2009). Thus, understanding their response to habitat
alteration is necessary to improve our forecasts regarding the
conservation of the species and also for the maintenance of
ecosystem integrity.
By combining field-based and Geographic Information
System (GIS) –based data, we aimed to identify the relative
importance of environmental variables describing the habitat
characteristics and anthropogenic disturbance factors affecting
the density of C. moreletii in nine wetlands in central Veracruz,
Mexico. We tested the expectation that a higher vegetation
complexity in terms of cover, richness, and structure may be
related to a higher relative density of crocodiles, because of the
importance of complex habitats for nesting and refuge against
predators. Additionally, if road density does indeed reduce the
persistence of crocodile populations, we hypothesized that there
was a negative relationship between road density and the
relative density of crocodiles. Finally, because crocodiles are
189
found commonly in areas near the shoreline, we expected that
the relationships between relative density of crocodiles and
vegetation complexity and road density would be stronger in
the immediate proximity of the water body and disappear as
distance to the water body increased.
MATERIALS AND METHODS
Study Species.—Crocodylus moreletii is distributed in the
Caribbean and the Gulf of Mexico. Owing to the depletion of
their population by historical hunting, this species has received
special protection from IUCN (2011), CITES (Appendix II;
CITES, 2010), and the Mexican government (SEMARNAT, 2010).
Because crocodile hunting has been forbidden since the 1970s,
the conservation status of C. moreletii has changed recently to
promote its controlled commercialization on the basis of the
recovery of local populations (CITES, 2010; CONABIO, 2010).
However, despite the economic and ecological importance of
crocodiles (Thorbjarnarson, 1999), information on the effects of
habitat alteration on crocodile populations remains very scarce
and is largely contradictory (Ouboter and Nanhoe, 1988; Platt
and Thorbjarnarson, 2000; Tews et al., 2003).
Study Area.—The Veracruz coastal plain is located in the
southern portion of the Gulf of Mexico. This area is character-
ized by a warm and humid climate (mean annual temperature
of 258C and an annual rainfall between 600 and 2,500 mm). The
original dominant vegetation was lowland tropical forests and
mangroves, but this region has been severely deforested and
fragmented, and the wetlands are now mostly surrounded by
farmlands (e.g., agricultural and pasture lands). On the central
coastline of the state of Veracruz, we randomly selected nine
wetlands previously detected by remote perception with the use
of a GIS. From north to south, these wetlands included Ciénegas
del Fuerte Popal (CFP), Ciénegas del Fuerte Selva (CFS), Estero
Dulce (ED), Casitas (CS), Laguna Chica (LC), La Mancha (LM),
San Julián (SJ), Rı́o Caña (RC), and Popotera (PO) (Fig. 1).
Characteristics of Wetlands.—The nine selected wetlands
averaged 3,280.4 ha (ranging between 25.1 and 12,090.2 ha).
CFS, ED, CS, LM and RC represented open wetlands (i.e., rivers
or creeks) and CFP, LC, SJ, and PO represented closed wetlands
(i.e., lagoons, oxbow lakes, or ponds). Within each wetland, we
evaluated 48 environmental properties (Appendix 1; available
online at http://dx.doi.org/10.1670/12-150s1): 1) physicochem-
ical and physical water body variables, including depth, pH,
salinity, and size; 2) biological variables composed of vegetation
composition and structure at the border of each water body; and
3) anthropogenic variables such as road type, road density, and
proportion of vegetation cover. The former variables (anthro-
pogenic) have been reported as potential hazards or stressors
for other crocodile populations (Vos and Chardon, 1998;
Fennessy et al., 2004).
The pH and salinity of the water bodies were measured at a
30-cm depth within each water body at 6–12 equidistant points
per site located near the shoreline with the use of a multi-
parametric instrument (YSI 63, YSIt, OH). To assess the
vegetation composition and structure at the border of each
water body, we sampled all the herbaceous and woody plant
species in five 100-m linear transects perpendicular to the edge
of the water body with a minimal separation of 50 m between
transects. The vegetation density and richness were measured
with the use of the Braun-Blanquet index (Matteucci and Colma,
1982; Clevenger and Waltho, 2000). To evaluate the density and
species richness of woody vegetation, we placed three 10 · 10–
190 R. GONZÁLEZ-TRUJILLO ET AL.
m plots in each transect separated by 50 m. Within each plot, we
placed three 2 · 2–m plots randomly to evaluate the herbaceous
coverage. Specimens of all species were collected for identifica-
tion at the XAL herbarium (Instituto de Ecologı́a, A.C., Xalapa,
Veracruz). To evaluate the vertical vegetation structure in each
10 · 10–m plot, we measured the height of each individual with
diameter at breast height >2 cm, and height was binned in
categories of 2 m.
We modeled three concentric buffer zones around each water
body (Semlitsch and Bodie, 2003) with the use of ArcView 3.2
(Environmental Systems Research Institute [ESRI], 1998) on the
basis of a set of orthophotos from Veracruz State (1:75,000;
INEGI, Mexico). The first buffer zone was termed the core zone
and included a band 12 m in thickness at the edge of the water
body; this is the zone where Morelet’s crocodiles locate most of
their nests (Hall, 1991; Platt and Thorbjarnarson, 2000). From
the core zone to the inland zone, we established two additional
terrestrial buffer zones (12–220 m and 220–831 m) that
correspond to the total habitat of crocodiles and other
semiaquatic reptiles (Hall, 1991; Burke and Gibbons, 1995; Platt
and Thorbjarnarson, 2000; Casas-Andreu, 2003; Schabetsberger
et al., 2004).
Finally, we estimated the density of roads per wetland (km-1)
and land-use cover (%) with the use of 10 buffers of 831 m with
their centers at 10 points per water body with the use of Arc
View 3.2. To calculate road density within each buffer zone and
wetland, we considered two road types: paved and nonpaved
(Dodd et al., 1989; Findlay and Houlahan, 1997; Rytwinski and
Fahrig, 2012). In the case of paved roads, we multiplied road
density by two, which is a modification of the methods of Vos
and Chardon (1998) and Forman (2000), to account for the
potentially higher impact of paved roads because of road killing
(Reijnen et al., 1995, 1996). Because roads located closer to the
body of water may have a greater influence on crocodile
populations than those located far away, we ranked the buffer
zones based on distance to the shoreline (Findlay and
Houlahan, 1997). We modified the Findlay and Houlahan
(1997) methods to assess the impact of road density at different
distances from the shorelines; i.e., road density was multiplied
by 3 if the road was within 12 m from the shore, and by 2 if
roads were present between 12 and 220 m from the shore, and
no correction factor was employed for roads present after 220 m.
We considered four land-use categories based on Knutson et al.
(1999) and Carr and Fahrig (2001), and we tested their
correspondence to the main dominant vegetation types in each
selected wetland on the basis of vegetation ordination, namely,
agricultural lands, rangelands, and cultivars (MO), mangrove
swamps (MA), flooded forest (FO), and freshwater marsh (FM).
These categories were confirmed in the field by verifying that
the land use was concordant with the information provided by
the GIS with the use of the same points of the vegetation survey.
Survey Methods.—Between May 2005 and May 2006, we
performed at least three nocturnal spotlight surveys per
wetland. The relative density (RD) of crocodiles was estimated
as the number of individuals observed per kilometer of survey
route (Seijas and Chávez, 2000) to control for differences in
water-body size. The length of each survey was calculated with
the use of 1:75,000 digital orthophotos in Arc View 3.2.
Although the density of plants could bias the rate of sightings,
Bayliss (1987) and Platt and Thorbjarnarson (2000) noted that
the rate of encounters is nearly constant across vegetation types,
which is a typical assumption in spotlight counts. We followed
the Platt and Thorbjarnarson protocol (2000), and classified the
individuals into three size classes (class I: <100 cm, class II: 100–
150 cm, class III: >150 cm).
Data Analyses.—The crocodile size categories did not show
significant differences within each wetland with the use of a
nonparametric analysis of variance (Kruskal-Wallis test) with
the exception of the CS wetland, which was dominated by class
II individuals (H = 8.52; P = 0.01). Therefore, we merged all
individuals to obtain a single RD of crocodiles per locality
(Seijas and Chávez, 2000; Stirrat et al., 2001). The physicochem-
ical properties of the wetlands were compared using a one-way
ANOVA. We calculated the Shannon-Wiener diversity index for
each plant community using the Species Diversity and Richness
IV software (Seaby and Henderson, 2006), and we created a
vertical vegetation structure of the Shannon-Wiener habitat
diversity index (Onaindia et al., 2004) using the frequency of
individuals in each height category. Using plant species richness
and abundance data, we grouped the wetlands by vegetation
type based on a nonmetric multidimensional scaling ordination
(NMS) with Sorensen distance algorithm (Bray and Curtis) with
PC-ORDv5 software (McCune and Mefford, 1999). Once the
wetlands were classified according to the NMS, we examined
the relationships between the RD of crocodiles and the locality
and wetland types with a Kruskal-Wallis test.
Finally, we applied simple linear Pearson correlations to relate
the RD with the environmental (i.e., physicochemical charac-
teristics of the water bodies as well as diversity and vertical
structure indices) and landscape variables (i.e., density of roads
and proportions of different land covers). To summarize the
patterns of covariation and reduce multicollinearity in the 48
variables explaining vegetation and landscape characteristics,
we used a principal-components analysis (PCA). The first and
second principal components were correlated with the relative
density of crocodiles, and we examined their variation across
vegetation types using a one-way ANOVA.
RESULTS
Characteristics of Water Bodies.—The depth of the water bodies
ranged from 1 to 4 m, the pH ranged from 7.31 to 8.03, and the
water salinity ranged from 0 to 16.3 ppt (Table 1). The width of
the water bodies was between 2.7 and 692 m (Table 1). All of
these variables differed significantly among sites (depth: F8,85 =
39.4, P < 0.001; pH: F8,85 = 22.9, P < 0.001; salinity: F8,85 = 55.6,
P < 0.001; and water body width: F8,85 = 208.8, P < 0.001).
Given that the area of the water bodies was not correlated with
the relative density of crocodiles (r = 0.13, P = 0.73) and that no
significant differences in the density of crocodilians were
observed between open and closed wetlands (t = 0.77, P =
0.45), these two factors were excluded from further analysis.
We identified 166 plant species (69 woody and 97 herbaceous)
belonging to 138 genera and 61 families (Table 1, Appendix 2
[available online at: http://dx.doi.org/10.1670/12-150s2]). Ac-
cording to the NMS analysis, our study sites were classified into
four categories of vegetation (FS statistic = 17.47, P = 0.01;
Appendix 3 [available online at: http://dx.doi.org/10.1670/
12-150s3]): 1) mangroves (CS, LC, and LM sites), dominated by
Avicennia germinans, Rhizophora mangle, and Laguncularia race-
mosa; 2) forests (CFS and ED sites), characterized by Pachira
aquatica and Annona glabra; 3) freshwater marshes (CFP, RC, and
PO sites), dominated by herbaceous vegetation such as Typha
latifolia, Sagittaria lanceolatta, Thalia geniculata, and Pontederia
sagittata; and 4) modified vegetation (SJ site), characterized by
Bursera simaruba, Coccoloba uvifera, and Daphnopsis americana
 HABITAT SUITABILITY FOR CROCODYLUS MORELETII 191
TABLE 1. Characterization of nine water bodies in central Veracruz, Mexico based on physicochemical and vegetation variables. We also indicate the relative density of C. moreletii populations and

Relative density

(mean 6 SD)

1.33 6 1.55

0.52
0.84
0.28
0.34
6.34
0.11
(ind
km-1)

6
6
6
6
6
6
0
0
0.61
0.27
3.66
3.35
1.4

4.89
Crocodiles

43.8 10.5
34.1 65.9
III

25
0
71.4 0
87.5 0

0
0
categoriesd (%)
Size

II

50

50
0

0
0
28.6
0.15 12.5
0.57 45.7
0.76 100
50

0.49 25

0
0
0
I

0.14
Cover

1.1
(%)

100

100
100
(ind
m-2)
Density

0.176
0.34
0.22
0.15
0.28
0.11
1

1
1
structure (H)
Vertical

1.71
1.47
1.81
1.79
0.91
1.9
0

0
0

FIG. 2. Relative density (RD) of crocodiles between vegetation

categories (H = 16.5, df = 3, P < 0.001). MA = mangrove (CS, LC,
1.77
1.73
2.21
1.43

2.51
2.97

and LM sites), FM = freshwater marsh (CFP, RC, and PO sites), FO =

2.3

2.8
h

forest (CFS and ED sites), and MO = modified category (SJ site). Lower-
Vegetation

Diversityc

case letters within the figure indicate significant differences in RD.

0.939
1.06

2.76
2.27
1.79
1.36

2.86
0.69
0.47
w

(Appendix 2). The forest sites had the highest total species
2.74
2.73
2.12
0.93
3.38
3.03
2.94
3.11
2.5
T

richness and diversity, followed by the freshwater marsh and

mangrove sites (Table 1). The mangrove and forest were the
20

18
10
20

19
5

23
0

21
h
Species richnessb

most diverse in terms of vertical structure; i.e., the plants were

distributed fairly equally among the height strata (Table 1). In
26
13
4

11

30
7
3
2
2
w

contrast, a single layer of vegetation dominated the freshwater

marsh; therefore, this area had the lowest diversity in terms of
24

44
23
31
12

49
25
23
3
T

vertical structure. In contrast, the freshwater marsh was the

richest and most diverse in terms of herbaceous species
wetlanda
Type of

followed by the forest and mangrove. The species richness

MO
MA
MA
MA
FM

FM
FM
FO
FO

and diversity was higher in the modified wetland (Table 1).

Habitat Attributes Affecting Crocodile Populations.—There were
According to Platt and Thorbjarnarson (2000); I: <100 cm; II: 100–150 cm; III: >150 cm.
River width (m)

13.48
139.6

significant differences in crocodile RD among wetlands, which

(mean 6 SD)

11.1 6 4.08

0.27
16.4

17.5
8.19
5.12
2

was previously square-root transformed to improve its normal-

Physicochemical characteristics of each water body

6
6
6
6
6
6
6
6

ity and heteroscedasticity between localities (n = 76, KW, H =

2.7

692
8.1
33
16.8
110.7

32.2
25.5

T = total number of species, w = woody species, h = herbaceous species.

32.9, df = 8, P < 0.0001). The physicochemical characteristics of

FM = freshwater marsh, FO = forest, MA = mangrove, MO = modified.

the study sites were not related to the crocodiles’ RD (depth, r =

1.14
6.73
0.15
1.56
0.01
(mean 6 SD)
Salinity (ppt)

-0.28, P = 0.5; pH, r = 0.14, P = 0.7; salinity, r = 0.2, P = 0.5;

width, r = 0.39, P = 0.3). RD varied significantly among
0.11 9.73 6
0.09 4.09 6
0.31 0.06 6
0.13 16.33 6
0.06 0.25 6
0

0
0

vegetation types, being significantly lower in the freshwater

marshes in comparison with mangroves; however, RD did not
vary between mangroves, forests, and modified vegetation (H =
(mean 6 SD)

7.31 6 0.19

0.18

0.22
0.4

16.50, df = 3, P = 0.0009; Fig. 2). RD was also related positively

pH

6
6
6
6
6
6
6
6
the percentage of individuals per size class.

to the vertical structure of vegetation (r = 0.33, P = 0.01); i.e.,

7.46
7.96
7.93
7.83
8.03
7.39
7.7
7.5

more animals were found when all the strata of vertical

H = Shannon-Wiener diversity index.

vegetation were present, which occurred in the mangrove and

(mean 6 SD)

3.86 6 0.16

0.05
0.41
0.82

0.16
1.36
0.09
Depth (m)

0.7

forest areas (Tables 1 and 2). RD was also negatively related to

0
6
6
6
6
6
6

herbaceous species richness (r = -0.62, P < 0.001). Finally, we

6
6
0.97
3.08
3.01
1.5
2.5
1.2
2.4
1.1

found that RD was correlated negatively with the density of

nonpaved roads in the core zone (r = -0.24, P = 0.02). Roads
Abbr.

CFP

CFS

were present in nearly all of buffer zone 1 and 2 (12–220 m and

LM
ED

RC
PO
LC
CS

SJ

220–831 m; Appendix 5, available online at http://dx.doi.org/

Fuerte-Popal

Fuerte-Selva

10.1670/12-150s5), but their presence was not significantly

Laguna Chica
Ciénegas del
Ciénegas del
Estero Dulce

correlated with the RD of crocodiles (Appendix 4, available

La Mancha
San Julián
Rı́o Caña
Site

Popotera

online at http://dx.doi.org/10.1670/12-150s4). The agricultural

Casitas

cover was unrelated to RD (r = -0.02, P = 0.95; r = 0.12, P =

d
b
a

0.75; r = 0.34, P = 0.36 for the core, first, and second buffer
192 R. GONZÁLEZ-TRUJILLO ET AL.

TABLE 2. Eigenvalues (k), percentage of explained variance (%), and Pearson linear correlations for the first and second principal-component axes
summarizing 48 variables related to anthropogenic modification as well as vegetation composition and structure in nine coastal lagoons in central
Veracruz, Mexico.

PC1 (k = 18.35, 38.2%) PC2 (k = 11.94, 24.9%)

Variable r P r P
-2
Plant density (ind
m ) -0.95 <0.001 0.07 0.84
Diversity of herbaceous species (H) -0.91 <0.001 -0.20 0.60
Vertical vegetation structure (H) 0.82 <0.01 -0.40 0.30
Total plant richness -0.31 0.40 -0.71 0.03
Diversity of woody species 0.36 0.33 -0.69 0.03
Cover of forest in the core zone (%) 0.96 <0.001 -0.12 0.77
Cover of forest in the second buffer (12–220 m, %) 0.69 <0.05 -0.37 0.33
Cover of freshwater marsh in the core zone (%) -0.97 <0.001 0.13 0.73
Cover of freshwater marsh in the second buffer zone (12–220 m, %). -0.91 <0.001 0.09 0.82
Road density outside the core zonea 0.58–0.52 0.1–0.76 0.79–0.87 <0.01 in all cases
a
Includes eight paved and unpaved road density variables for the second (12–220 m) and third (220–831 m) buffer zones.

zones, respectively; Appendix 4). We found that 7 of 48 that up to 44% of nests are built in the forested banks of the
landscape and vegetation variables were correlated with the lagoons, any well-preserved strip of arboreal vegetation should
RD of crocodiles (Appendix 4). The first and second principal benefit the reproduction of this species (Knutson et al., 1999;
components explained 38.2% and 24.9% of the variance in our Platt and Thorbjarnarson, 2000). For hatchlings, arboreal
data set, respectively (Table 2). We extracted the first and second vegetation can increase hatchling density by providing protec-
principal components, which were correlated with five land- tion against predators and high temperatures (Cedeño-Vázquez
scape metrics and five vegetation metrics (Table 2). We found et al., 2006). Even for adult crocodiles, a forested margin can act
that the first principal component was correlated with the RD as a shelter against predators, including humans (Herron, 1994;
(Fig. 3). The first principal component also varied based on Knutson et al., 1999).
vegetation type (F2,8 = 20.10, P = 0.003); however, the second We found that density of crocodiles is also related to
principal component did not vary across vegetation type (F2,8 = vegetation type and tree structure. For example, mangrove
2.97, P = 0.13). was the forested habitat that harbored the largest population of
C. moreletii, likely because of its complex vertical structure
DISCUSSION (reaching a height of greater than 15 m). Moreover, as mangrove
Overall, our findings indicate that on the Veracruz coastal is less accessible for humans than any other vegetation type, it
plain, arboreal vegetation at the edge of water bodies is a provides refuge against hunting (Cedeño-Vázquez et al., 2006).
particularly favorable habitat for crocodiles. In fact, our results In contrast, in freshwater marshes, the relative density of
suggest that as long as the water bodies are bordered with crocodiles was low, which was likely related to the lack of
arboreal vegetation, land-use change and the density of paved
roads in inland areas may result in only minor impacts on
Morelet’s crocodile populations in Mexican wetlands.
The Role of Vegetation in the Establishment and Persistence of the
Morelet’s Crocodile.—Arboreal vegetation is a critical component
of habitat quality for the Morelet’s crocodile. Our GIS-simulated
buffer zones suggest that the minimum width of arboreal
vegetation is approximately 12 m inland. This result agrees with
that reported for Crocodylus acutus in Panama (Rodda, 1984).
Although a relatively small area of forested banks appears to be
adequate for the maintenance of crocodile populations, even a
slight change in arboreal vegetation surrounding the borders of
the water bodies may be associated with a reduction in the
number of crocodiles. The values of RD found in our study
(0.61–4.89; Table 1) are within the ranges reported in the
literature. In comparison, Cedeño-Vázquez et al. (2006) ob-
served densities ranging from 0.87 to 7.57 ind
km-1 in southern
Mexico, and Platt and Thorbjarnarson (2000) observed densities
ranging from 0.95 to 6.11 ind
km-1. These authors postulated
that variation in RD occurs because of diverse habitats, as more FIG. 3. Relationship between the first principal component (PC1)
from a principal-component analysis and the relative density of
animals were observed in inaccessible wetlands with more crocodiles (square-root transformed) in nine Veracruz wetlands. PC1
vegetation such as marshes and swamps. Our findings are explained 38.2% of the variance and summarizes 48 characteristics,
consistent with this idea because the increase in RD with the including physicochemical conditions, vegetation diversity and
proportion of forested margins in our study sites can be related composition, and land-use changes. Study sites: Ciénegas del Fuerte
Popal (CFP), Ciénegas del Fuerte Selva (CFS), Estero Dulce (ED), Casitas
to the high availability of microhabitats in these areas, which (CS), Laguna Chica (LC), La Mancha (LM), San Julián (SJ), Rı́o Caña
facilitate the construction of nests by C. moreletii and provide (RC), Popotera (PO). Circles represent mangroves, squares = freshwater
leaf litter for construction and protection (Gibbs, 1998). Given marshes, triangles = forests, diamond = modified vegetation.
 HABITAT SUITABILITY FOR CROCODYLUS MORELETII
shaded areas and the extremely high densities of herbaceous
plants on the shorelines of lagoons, a condition that likely
increases nest exposure and limits thermoregulation (Clevenger
and Waltho, 2000). We also found that Morelet’s crocodiles can
persist in forested wetlands surrounded by croplands, which
was observed previously by Platt and Thorbjarnarson (2000) for
crocodile populations located in various water bodies in Belize.
The Role of Roads and Urbanization on Morelet’s Crocodile
Populations.—Crocodile density was related negatively to
human disturbance near water bodies, particularly in relation
to increasing road density. Consistent with our predictions, we
observed a negative relationship between the relative density of
crocodiles and road density close to water bodies. This finding
could be the result of behavioral avoidance of roads and/or the
effects of killing because of collisions with vehicles on roads.
Both factors limit dispersal movements and can affect the
persistence of populations (Findlay and Bourdages, 2000;
Trombulak and Frissell, 2000; Carr and Fahrig, 2001; Gibbs
and Shriver, 2002; Fahrig and Rytwinski, 2009; Rytwinski and
Fahrig, 2012). In fact, roads represent an important factor in
habitat fragmentation as urbanization persists, particularly in
coastal areas (Martı́nez et al., 2006). Although the density of
roads and agricultural lands at a distance of 220–831 m from the
water bodies is not related negatively to crocodile abundance,
an increase in the human colonization of these water bodies
could likely push crocodiles to smaller vegetated areas, forcing
them to breed in grasslands or in floating nests and affecting
hatchling survival (Villegas-Castillo, 2011).
Therefore, we can conclude that our results represent a
further step toward the conservation of this species, as they
highlight the need for conservation of the strip of arboreal
vegetation at the borders of lagoons to preserve the Morelet’s
crocodile habitat. We suggest that the structure of the vegetation
and the density of roads at the borders of water bodies can be
used as adequate indicators of habitat suitability for this species
and other semiaquatic species under the same pressures.
Acknowledgments.—We thank B. Martı́nez-de León for assis-
tance during sample collection, J. P. Esparza-González for GIS
assistance, and Miguel Munguı́a for his helpful comments and
suggestions on an earlier version of this manuscript. This work
is presented by RGT as a partial fulfillment for obtaining a Ph.D.
at the Instituto de Ecologia, AC. RGT was supported by a
CONACYT doctoral fellowship (172256) and by the Red de
Biologı́a y Conservación de Vertebrados del Instituto de
Ecologı́a A.C. Field work was conducted under a special
collecting permit (SGPA/DGVS/02227 and SGPA/DGVS/
05851/07) given to AGR.
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