Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e31785, enero-diciembre 2023 (Publicado Mar. 30, 2023)

Deforestation increases the abundance of rodents and

their ectoparasites in the Lacandon forest, Southern Mexico

María Lourdes Barriga-Carbajal1; https://orcid.org/0000-0001-5118-8670

Margarita Vargas-Sandoval2; https://orcid.org/0000-0002-4835-8779

Eduardo Mendoza1*; https://orcid.org/0000-0001-6292-0900

1. Instituto de Investigaciones sobre los Recursos Naturales, Universidad Michoacana de San Nicolás de Hidalgo, Av.

San Juanito Itzícuaro s/n, Morelia 58337, Michoacán, México; lourdes.barriga@umich.mx,

eduardo.mendoza@umich.mx (*Correspondence)

2. Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo. Gral. Francisco J. Múgica S/N A-1,

Felicitas de Río, 58030. Morelia, Michoacán México; margarita.vargas@umich.mx

Received 30-VI-2022. Corrected 05-XII-2022. Accepted 23-III-2023.

ABSTRACT

Introduction: Tropical forests provide important ecosystem services, including disease control. However, few

studies have focused on how deforestation affects species more suitable to be zoonotic vectors.

Objective: To evaluate how deforestation affects the abundance and species richness of rodents and their associ-

ated ectoparasites in a tropical ecosystem.

Methods: We captured rodents in 6 landscape units, 1 km² each, with 0.7; 5; 40; 46; 78 and 95 % tree cover,

in Marques de Comillas, Chiapas, Southern Mexico. In each unit we set 90 Sherman traps that were active 24

hours for 7 days during two sampling seasons (October 2019, and September 2020). We manually extracted

ectoparasites from all captured rodents.

Results: We captured 70 rodents of five species: Sigmodon toltecus, Heteromys desmarestianus, Ototylomys

phyllotis, Peromyscus mexicanus, and Oryzomys couesi. Rodent abundance increased with forest loss (R²=

0.706, P= 0.022). The greatest richness of rodent species occurred in sites with intermediate forest cover (40

and 78 %). The most abundant species were: S. toltecus (N= 45) followed by O. couesi (N= 9), these species

dominated in sites with less forest cover. We recorded a total of 23 ectoparasite species, three of them known to

be zoonotic vectors: Amblyomma sp., Ornithonyssus bacoti, and Androlaelaps fahrenholzi.

Conclusions: The ongoing loss of forests promotes the proliferation of zoonotic disease vectors in this tropical

ecosystem, which can potentially increase the frequency of affectation among the local population.

Key words: deforestation; tropical forest; zoonoses; mites; reservoirs; vectors.

RESUMEN

La pérdida de bosques aumenta la abundancia de roedores y sus

ectoparásitos asociados en la Selva Lacandona, sur de México

Introducción: Un servicio particularmente importante que brindan los bosques tropicales es el control de

enfermedades. Sin embargo, pocos estudios se han enfocado en analizar cómo este servicio es afectado por la

deforestación.

Objetivo: Evaluar el efecto de la deforestación en la abundancia y riqueza de especies de roedores y de sus

ectoparásitos en Marqués de Comillas, en el sureste de México.

https://doi.org/10.15517/rev.biol.trop..v71i1.31785

TERRESTIAL ECOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e31785, enero-diciembre 2023 (Publicado Mar. 30, 2023)

INTRODUCCIÓN

Human activities are causing a drastic

transformation of tropical forests due to the

proliferation of land dedicated to monocul-

tures, commercial plantations, cattle pasture,

and the overexploitation of plants and animals

(Dirzo et al., 2014; Gayley & Sridith, 2020).

These modifications directly affect the wealth

of ecosystem services provided by tropical

forests (Brockerhoff et al., 2017). There has

been intense debate regarding the role played

by biodiversity in reducing or increasing infec-

tious disease risk (Rohr et al., 2020). However,

recent studies tend to agree with the idea that

biodiversity loss appears to raise the risk of

human exposure to zoonotic pathogens as a

consequence of increases in the abundance of

species that are particularly suitable to be zoo-

notic hosts (Keesing & Ostfeld, 2021). There

is a need for research focused on analyzing the

response species sharing zoonotic pathogens

with humans have to the most common human

activities affecting tropical forests, such as

deforestation (Guégan et al., 2020).

Rodents are of great relevance in tropi-

cal forests due to their abundance and variety

of ecological roles, such as seed dispersers

and predators (Vélez & Pérez, 2010). Some

rodent species seem to withstand the effects of

human perturbations most commonly affecting

tropical forests and even, in some instances,

benefit from the conditions associated with

anthropized landscapes (Mendoza et al., 2020;

Morand et al., 2019). In contrast, some species

have small distribution ranges and special-

ized habits that makes them more prone to

be negatively impacted by tropical forest per-

turbation (Mendoza & Horváth, 2013; Rubio

et al., 2014). Small rodents interact with an

important number of arthropods in the orders

Ixodida (ticks), Mesostigmata (facultative para-

site mites), Trombidiformes (free-living mites,

parasites in larval stage), Sarcoptiformes (com-

mensal and parasite mites) as well as insects

in the orders Siphonaptera (fleas), Phthiraptera

(lice) and Heteroptera (bugs) (Guzmán et al.,

2020; Madinah et al., 2014). Despite the known

role of these arthropods as ectoparasites reser-

voirs and vectors of pathogens (e.g., viruses and

bacteria) there is little information on how they

are affected by habitat perturbation (Guzmán et

al., 2020; Ramalho & Gubler, 2020).

Tropical forest perturbation can affect the

prevalence of rodent ectoparasites through dif-

ferent pathways. First, the impacts of forest

perturbation on the abundance of rodent popu-

lations and the composition of their communi-

ties can in turn affect host availability (Ladds,

2015; Ssuuna et al., 2020). Second, habitat

Métodos: Capturamos roedores en 6 unidades del paisaje (UP), cada una de 1 km², con distintos porcentajes de

cobertura vegetal (0.7, 5, 40, 46, 78 y 95 %). En cada UP colocamos 90 trampas Sherman, que permanecieron

activas las 24 horas por 7 días durante dos muestreos en octubre 2019 y septiembre 2020. Todos los roedores

capturados fueron revisados para detectar ectoparásitos en su pelaje que fueron recolectados para su posterior

identificación en el laboratorio.

Resultados: Capturamos 70 roedores de cinco especies: Sigmodon toltecus, Heteromys desmarestianus,

Ototylomys phyllotis, Peromyscus mexicanus y Oryzomys couesi. La abundancia de roedores aumentó con la

pérdida de bosque (R² = 0.706, P = 0.022). La mayor riqueza de especies de roedores se presentó en sitios con

cobertura forestal intermedia (40 y 78 %). Las especies más abundantes fueron: S. toltecus (N = 45) seguido de

O. couesi (N = 9), estas especies dominaron en los sitios con menor cobertura forestal. Registramos un total de

23 ectoparásitos diferentes, identificamos 15 a nivel de especie y ocho a nivel de género. Los sitios con menor

cobertura forestal presentaron la menor riqueza de especies de ectoparásitos. Detectamos tres especies de ecto-

parásitos (Amblyomma sp., Ornithonyssus bacoti y Androlaelaps fahrenholzi) que se sabe que son vectores de

enfermedades zoonóticas.

Conclusión: Encontramos que la deforestación está promoviendo un aumento en la proliferación de vectores de

enfermedades zoonóticas lo que, a su vez, tiene el potencial de incrementar las afectaciones de la población local.

Palabras clave: deforestación; bosques tropicales; zoonosis; ácaros; reservorios; vectores.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e31785, enero-diciembre 2023 (Publicado Mar. 30, 2023)

perturbation can affect the physiological condi-

tion of rodents (e.g., stress levels) making them

more prone to be parasitized, or can directly

affect the species composition and population

abundance of ectoparasites due to the associ-

ated changes in abiotic factors such as humid-

ity and temperature (Hammond et al., 2019;

Rynkiewicz et al., 2013).

Tropical forests frequently support human

populations with high levels of poverty (Fisher

& Christopher, 2007). It is, therefore, an issue

of prime relevance to document the impacts

of tropical deforestation on rodent popula-

tions and the corresponding consequences for

ectoparasite abundance and diversity to prevent

zoonosis affecting people particularly vulner-

able. Moreover, research on this issue will help

to further our understanding of the ecosystem

service tropical forests provide for disease

control and how it responds to anthropogenic

perturbation (McMurray et al., 2017).

Our goals were: a) evaluating the rela-

tionship between forest loss and rodent spe-

cies richness and abundance, b) assessing the

associate effects on the abundance of rodent

ectoparasites and their species richness and

composition, and c) documenting the presence

of ectoparasites of zoonotic relevance such as

ticks, fleas, lice, and hematophagous mites. We

expect to find a reduction in the overall rodent

species diversity as forest extent reduces, due

to the increase in the abundance of species

adapted to live in transformed habitats. This

will be reflected in a greater abundance of the

associated ectoparasites. Among the species of

ectoparasites increasing their abundance, we

expect to find some species identified as vec-

tors of zoonotic diseases.

MATERIALS AND METHODS

Study site: This study was conducted in

the Marques de Comillas (MC) region which

is part of the Lacandon forest in the state of

Chiapas, Southern Mexico. The MC region has

an extent of 94 266 km² (INAFED, 2010). It is

limited to the West and North by the Lacantún

river, to the South by the Guatemala border,

and to the East and North by the Salinas river

(Fig. 1). The Montes Azules biosphere reserve

is located towards the west, covering an extent

of 331 200.00 ha (Carabias et al., 2000). The

mean annual precipitation in the region is 3 000

mm and the mean temperature is 24 °C (Mar-

tínez et al., 2009).

The Lacandon forest, together with its

natural prolongation in Belize and Guatemala,

constitutes one of the largest remnants of tropi-

cal rainforests in Mesoamerica (Cruz et al.,

2004). Unfortunately, over a period no longer

than 12 years, the Lacandon forest lost approxi-

mately 142 000 ha, accumulating a total loss of

nearly 70 % of its original extent (Carabias et

al., 2015; de la Torre & Medellín, 2011). Cur-

rently, this region supports a mosaic of remnant

native forests, secondary forests, cattle pas-

tures, and African palm plantations (Muench &

Martínez, 2016).

Selection of sampled landscape units:

Wies et al. (2021) estimated the percentage

of forest cover in 18 landscape units of 1 km²

within the MC, using Sentinel-2 satellite imag-

es, with a 10 m spatial resolution, and ground-

truthing. Based on this information we selected

six sampling sites with different percentages of

forest cover (AT1).

Rodent capture: We set 90 Sherman traps

in each LU, along two parallel lines separated

by 20 m with a distance between consecutive

traps of 10 m. These traps remained active for

24 hours during 7 days, were baited daily with

a mixture of liquid vanilla and oat flakes, and

checked early every morning.

All the captured rodents were euthanized

by applying an overdose of pentobarbital sodic

in the intraperitoneal zone. This procedure

followed the guidelines for the ethical treat-

ment of animals from the American Society of

Mammalogists (Gordon & Kirkland, 1998). To

limit the number of rodents to be sacrificed we

reduced our sample size to the minimum num-

ber of six sites as indicated above. The sacri-

ficed individuals belonged to species not listed

as threatened at the national or global level.

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e31785, enero-diciembre 2023 (Publicado Mar. 30, 2023)

Ectoparasite sampling: We applied repet-

itive abrasive combing of the whole body of

each one of the sacrificed rodents with the help

of a toothbrush (Lareschi et al., 2019). More-

over, we conducted a visual search of ectopara-

sites attached to the skin of rodents and checked

the plastic bags where they were stored. All the

collected arthropods were deposited in a solu-

tion of Kono’s liquid for 7 to 30 days to disinte-

grate their internal organs and stomach content.

The resulting exoskeletons were mounted on a

slide with a drop of Hoyer’s solution to con-

duct taxonomic identification with the help of

specialized taxonomic keys (Bassols, 1975;

Fain & Lukoschus, 1984; Guzmán et al., 2011;

Stojanovich & Pratt, 1961).

Data analyses: We conducted a linear

regression analysis to assess the relationship

between forest cover (%) (mature + secondary

forest) and rodent abundance. To compare ecto-

parasite species richness among the LUs we

built accumulation curves using Hill number

q = 0. These curves were extrapolated to the

largest sample size, using as a sampling unit

the corresponding number of trapped rodents.

We calculated the 95 % confidence intervals for

each curve (Chao et al., 2014) using the iNEXT

package (Hsieh et al., 2019).

We generated a dendrogram to explore the

relationship among LUs based on their spe-

cies richness and abundance of ectoparasites.

Applying the procedure described in Borcard et

al. (2018), we produced a matrix of Euclidean

distances among sites based on the standard-

ized abundance (option “normalized”) of their

ectoparasites. We generated four dendrograms

using the single linkage, complete linkage,

UPGMA, centroid, and Ward´s minimum dis-

tance algorithms and calculated cophenetic

correlations and Gower distances to assess their

performance. Gower’s distance is a statistic

used to assess the comparative performance

of data grouping methods. It is calculated as

Fig. 1. Location of the study area in the Marques de Comillas region in the state of Chiapas, Southern Mexico. The stars

indicate the location of the sampled landscape units.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e31785, enero-diciembre 2023 (Publicado Mar. 30, 2023)

the sum of squared differences between origi-

nal and cophenetic distances. The grouping

method having the lowest Gower value is

taken as the one having the best performance

(Borcard et al., 2018). To conduct this analy-

sis, we used the package Vegan (Oksanen et

al., 2020). We excluded from this analysis the

rodent species Ototylomys phyllotis due to the

fact it was represented only by one individual

and in contrast with the other species recorded

is highly arboreal.

To examine the existence of differences

in the number of ectoparasites recorded on

Sigmodon toltecus among the different trap-

ping sites we applied a Kruskal-Wallis test

(Zar, 2010). Afterward, we applied a Dunn

test with Bonferroni’s adjusted probabilities to

identify which pairs of sites were statistically

different. The use of this test is recommended

in cases in which replication is not balanced

among treatment levels (Zar, 2010). To con-

duct these analyses, we used the package FSA

(Ogle et al., 2021). All the above analyses were

conducted using the software R ver. 3.6.3 (R

Core Team, 2020).

RESULTS

With a sampling effort of 3 780 trap days,

we captured a total of 70 rodents (overall 43

males and 27 females) belonging to five spe-

cies. The most abundant species was Sigmo-

don toltecus (N= 45), followed by Heteromys

desmarestianus (N= 9), Oryzomys couesi (N=

9), Peromyscus mexicanus (N= 6), and Ototy-

lomys phyllotis (N= 1). In the sites where the

forest coverage was the lowest, the abundance

of S. toltecus and O. couesi was the highest

(Fig. 2A). In contrast, the species P. mexicanus

and H. desmarestianus occurred only in the

Fig. 2. A. Rodent abundance in six 1 km2 landscape units, with different forest cover extents in the Marques de Comillas

region, Southern Mexico. Sigmodon toltecus (S.tol), Oryzomys couesi (O.cou), Peromyscus mexicanus (P.mex), and

Heteromys desmarestianus (H.des). B. Relationship between forest coverage and rodent abundance in the six 1 km2

landscape units sampled in the Marques de Comillas region in Southern Mexico. The shaded area corresponds to the 95 %

confidence interval for the regression.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e31785, enero-diciembre 2023 (Publicado Mar. 30, 2023)

sites with greater forest coverage (Fig. 2A).

None of the five rodent species occurred in

all six LUs.

The overall abundance of rodents was

inversely proportional to the percentage of for-

est cover (R²= 0.706, df= 5, P= 0.022). Thus,

the LUs with less forest cover (LM_0.7 % and

CHA_5 %) concentrated the greatest number of

rodents (25 and 17, respectively) whereas in the

LUs with the greatest forest coverage (CHP_78

% and PLR_95 %) only occurred five and three

rodents (Fig. 2B).

We identified 23 different ectoparasites,

15 of them at the species level and eight at the

genus level (AT2). The more abundant organ-

isms were mites in the families Listrophoridae

(Geomylichus nectomys, Prolistrophorus sp.,

Prolistrophorus bakery, and Prolistropho-

rus grassi) and Trombiculidae (Cordiseta

mexicana, Pseudoschoengastia brennani,

Parasecia kansasensis, Dermadelema moja-

vense, and Eutrombicula batatas). The less

abundant species was Gigantolaelaps boneti

(Laelapidae family).

The ectoparasite species accumulation

curves showed a trend towards stabilization

with the clear exception of site PLR_95 %;

however, this site had the smallest number of

rodents captured making the extrapolation of

limited value. There was a great overlap among

the 95 % confidence intervals of accumulation

curves but LUs GIL_46 % and CHP_78 %

Fig. 3. A. Accumulation curves of ectoparasite species in six sites with different percentages of forest coverage in the

Marques de Comillas in Southern Mexico. The shaded areas correspond to 95 % confidence intervals and dashed lines to

extrapolations. B. Comparison of the abundance of ectoparasites recorded in individuals of Sigmodon toltecus captured in six

1 km2 landscape units with different levels of forest coverage in the region of Marques de Comillas in the state of Chiapas,

Southern Mexico. * Sites statistically different based on Dunn the test (P < 0.05).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e31785, enero-diciembre 2023 (Publicado Mar. 30, 2023)

were located over the curves corresponding to

LUs LM_0.7 %, CHA_5 %, and PL2_40 %

(Fig. 3A).

There was a significant variation in the

number of ectoparasites among individuals of

S. toltecus captured (Chi² = 13.2, df = 3, P =

0.004, Fig. 3). Two sites were different LM_0.7

% and GIL_46 % (Dunn test, P = 0.0044). The

greatest ectoparasite abundance occurred in

the LU with the highest deforestation and the

lowest in the LU with 46 % forest coverage

(Fig. 3B).

The dendrogram using the UPGMA algo-

rithm had the highest cophenetic correlation

(0.846 vs. 0.840, 0.830, 0.782) and the lowest

Gower distance (0.401 vs. 1.036, 1.390, 3.037).

Sites were segregated into two main clusters.

The first one of them was constituted by the

sites with the lowest forest coverage. The

second main cluster was, in turn, divided into

two smaller clusters. The first one of these sub-

clusters included sites GIL_46 % and CHP_78

%, which had a relatively high species richness

of ectoparasites whereas the second included

sites PL2_40 % and PLR_95 % (Fig. 4).

DISCUSSION

In agreement with our predictions, we

found that rodent, and ectoparasite abundances

increase with forest loss. The rodent species

we recorded constitute approximately 50 %

of the total number of species recorded in the

Lacandon forest (Cruz et al., 2004). It would

be highly desirable to include surveys of the

canopy fauna in future studies to have a more

complete view of the impact forest loss is

having on the rodents and their associated

ectoparasites. We recorded the greatest species

richness of rodents in sites with intermediate

levels of forest coverage (GIL_46 % y CHP_78

%). This likely relates to the presence in these

sites of greater habitat heterogeneity associated

with the mixture of vegetation in different lev-

els of secondary succession, forest fragments,

crops, commercial plantations, and cattle pas-

ture (e.g., Ssuuna et al., 2020).

Species such as S. toltecus and O. couesi

likely benefit from the extensive transforma-

tion of the landscape in our study region due to

the fact they are omnivorous and include a vari-

ety of grasses and seeds in their diets. This can

help them to thrive in areas dominated by cattle

pastures and monocultures (Peña et al., 2009).

Moreover, these species have reduced gesta-

tion periods (no longer than one month) and

produce on average eight individuals per litter

(Ceballos & Oliva, 2005). In contrast, species

such as H. desmarestianus and P. mexicanus

are known to have the capacity to move across

areas with pasture or crops but their presence

tends to be more associated with mature forests

(Ceballos & Oliva, 2005).

We obtained some evidence that the

ectoparasite load increases with forest loss.

Fig. 4. Relationships among the six landscape units sampled in the Marques de Comillas, state of Chiapas, based on the

composition of the recorded ectoparasite fauna.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e31785, enero-diciembre 2023 (Publicado Mar. 30, 2023)

A similar effect was reported by Froeschke

et al. (2013) in fragmented forests in South

Africa. These authors suggest that this effect

relates to the fact that the conditions in the

transformed habitats offer greater availability

of resources such as water and a lower presence

of predators. These conditions can in turn favor

peridomestic rodents to reach a larger body

size and therefore to be able to carry a larger

number of ectoparasites.

Studies conducted in Mexico have detected

pathogens causing diseases such as leishmani-

asis, Chagas, rickettsiosis, and hemorrhagic

fever in all the rodent species we recorded in

this study (Lorenzo et al., 2017; Panti et al.,

2021). Ticks are very dangerous vectors due to

their hematophagous diet and need to have sev-

eral hosts to complete their life cycles (Main

& Bull, 2000; Stafford et al., 1995). Moreover,

other arthropod species we detected such as

Amblyomma sp., O. bacoti, and A. fahrenholzi

can be vectors of viruses and bacteria such as

Hantavirus, Flavirus, Rickettsia, Borrelia, and

Bartonella (Kabeya et al., 2010; Moro et al.,

2005). There is evidence that the increased

abundance of O. bacoti is associated with dis-

ease incidence in domestic animals and humans

(Beck & Fölster, 2009). There are no current

reports on human infections associated with A.

fahrenholzi however, the presence of Rickettsia

and Bartonella has been reported in Mexico

(Zapata et al., 2017).

We also recorded the presence of parasitic

larvae of arthropods in the order Trombidiformes

(C. mexicana, P. brennani, P. kansasensis, D.

mojavense, and, E. batatas). There are no records

of these species being associated with etiologi-

cal agents however, the larvae of other trombi-

culid species such as Neotrombicula autumnalis,

Microtrombicula sp. and, Leptotrombidium scu-

tellare are known to be vectors of pathogens

including Caulobacter yokenella and species in

the genera Actinomycetospora, Coxiella, and,

Bosea (Masakhwe et al., 2018). The parasitic

larvae of these genera cause important affec-

tations on health in both wild mammals and

humans by producing severe dermatitis (San-

tibañez et al., 2014).

We did not detect the presence of fleas

in the rodents. Fleas are of particular interest

due to the fact they can carry the pest vec-

tor Yersinia pestis (Carlson et al., 2022). The

continued monitoring of our study area will

help to discard the possibility that this lack

of detection of fleas is related to seasonal

variation in the abundance of these organisms

(Herrero et al., 2021).

It is important to highlight the fact that

not in all cases arthropods found in the fur of

small rodents are true parasites. Some arthro-

pod species take advantage of rodents for

transportation (phoresis) (Kim, 1985). These

species receive less attention due to the fact

they are not associated with disease transmis-

sion (Cornejo & Mares, 2021; Guzmán et al.,

2020). However, the study of this group of

species is needed to gain a deeper understand-

ing of the overall response of biodiversity to

anthropic perturbation.

From the different 23 groups of ectopara-

sites we recorded, we were only able to iden-

tify 15 at the species level and the remaining

eight at the genus level. In some instances,

samples corresponded to individuals in the

larval stage (e.g., Amblyomma sp.) complicat-

ing their taxonomic determination. Likewise,

mites belonging to the genus Echinonyssus

(species one to five), Prolistrophorus, and Der-

macarus had morphological traits that did not

match exactly those of the currently described

species, it exists the possibility they constitute

new species.

The health, social and economic impacts

of zoonotic disease associated with wild fauna

have generated great concern among scien-

tists, medical institutions, and people in gen-

eral (Saba & Balwan, 2021). However, more

research is still needed to identify the key fac-

tors favoring zoonosis spillovers (Stenvinkel et

al., 2021). In the meantime, it looks like one

of the best routes to prevent zoonosis is mak-

ing operative public policies and conservation

strategies focused on protecting tropical forests

and wildlife.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e31785, enero-diciembre 2023 (Publicado Mar. 30, 2023)

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

This study is a requisite for María Lourdes

Barriga-Carbajal to earn his degree in the

graduate program of Maestría en Ciencias

en Ecología Integrativa from the Universidad

Michoacana de San Nicolás de Hidalgo. María

Lourdes Barriga-Carbajal was supported by a

fellowship from the Mexican National Coun-

cil of Science and Technology (CONACyT)

and was advised by Eduardo Mendoza and

Margarita Vargas Sandoval. Eduardo Mendoza

and Margarita Vargas Sandoval were supported

by the Sistema Nacional de Investigadores

(SNI, National System of Researchers) while

conducting this research. We thank José María

Valdovinos, Marco Antonio Robledo, Michel

Ramírez and Carmina Domínguez for their

support in field work. Comments made by

Esperanza Meléndez H., Mariana Munguía C.,

and Clementina González Z., greatly improved

this study. Funding: This study was sup-

ported by grants from 1) CONACyT (Proj-

ect BIOPAS. SEP-CONACyT-2016-285840)

awarded to Miguel Martínez-Ramos and 2)

the Coordinación de la Investigación Cientí-

fica (CIC) from the UMSNH, awarded to

Eduardo Mendoza.

Ver apéndice digital /

See digital appendix - a14v71n1-A1

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