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Current status of dung beetles (Coleoptera, Scarabaeidae, Scarabaeinae)

diversity and conservation in Natural Protected Areas in Chiapas (Mexico)

Article in Neotropical Biology and Conservation · July 2020

DOI: 10.3897/neotropical.15.e53762

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 Neotropical Biology and Conservation
15(3): 219–244 (2020)
doi: 10.3897/neotropical.15.e53762

RESEARCH ARTICLE

Current status of dung beetles (Coleoptera,

Scarabaeidae, Scarabaeinae) diversity
and conservation in Natural Protected
Areas in Chiapas (Mexico)

Gibrán Sánchez-Hernández1, Benigno Gómez1,

Eduardo Rafael Chamé-Vázquez2, Rolando A. Dávila-Sánchez3,
M. Edivaldo Rodríguez-López1, Leonardo Delgado4

1 Conservación de la Biodiversidad, El Colegio de la Frontera Sur, Periférico Sur s/n, María Auxiliadora, CP
29290, San Cristóbal de Las Casas, Chiapas, México
2 Ecología de Artrópodos y Manejo de Plagas, El Colegio de la Frontera Sur, Carretera Antiguo Aeropuerto
Km. 2.5, CP 37000, Tapachula, Chiapas, México
3 Ingeniería Ambiental, Environmental Protection and Control, CP 12049, col. Mántica, Managua, Nicaragua
4 Red de Biodiversidad y Sistemática, Instituto de Ecología AC, Carretera Antigua a Coatepec No. 351, CP
91070, Xalapa, Veracruz, México

Corresponding author: Gibrán Sánchez-Hernández ([email protected])

Academic editor: P. Nunes-Silva | Received 2 May 2020 | Accepted 18 June 2020 | Published 20 July 2020

Citation: Sánchez-Hernández G, Gómez B, Chamé-Vázquez ER, Dávila-Sánchez RA, Rodríguez-López

ME, Delgado L (2020) Current status of dung beetles (Coleoptera, Scarabaeidae, Scarabaeinae) diversity and
conservation in Natural Protected Areas in Chiapas (Mexico). Neotropical Biology and Conservation 15(3): 219–
244. https://doi.org/10.3897/neotropical.15.e53762

Abstract
Natural Protected Areas (NPAs) are consider adequate tools for biodiversity conservation. Currently
in Mexico there are 182 federal NPAs classified according to their management objectives. Chiapas is
the Mexican state with the highest number of decreed NPAs and also allocates one of the largest ter-
ritorial extensions for its protection. Unlike other taxa, and despite their proven ability to respond to
ecosystem changes, the study of dung beetles within Mexican NPAs has been underestimated, as they
are not considered as a priority group within their management and conservation programs. Based on
the review of information available in publications and database on dung beetles, a list of 112 species
and seven subspecies recorded in 16 of the 19 federal NPAs established in Chiapas is presented. The
species recorded by each NPA show a significant correlation with the number of publications, but a

Copyright Gibrán Sánchez-Hernández et al. This is an open access article distributed under the
terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original author and source are credited.
220 Gibrán Sánchez-Hernández et al.

low percentage of them correspond to studies with systematic samplings and most of the species re-
ported in several of the NPAs come from sporadic records, which prevents the study of several basic
and applied aspects of dung beetles in the region. Therefore, studies that extensively analyze the com-
munities of arthropod groups, such as the Scarabaeinae, are necessary to understand their response to
changes in the ecosystem at local and regional scale. It is advisable that these insects be included in the
previous justifying studies for the designation or establishment of NPAs and, in turn, considered in the
biological monitoring programs of these areas for their capacity as a bioindicator group.

Keywords
bioindicator, biological monitoring, corridor, Faunistic complex, management, NPAs

Introduction

Natural Protected Areas (NPAs) are considered the main tool for the conservation of
biological diversity worldwide (Bezaury-Creel and Gutiérrez Carbonell 2009). These
are defined as areas that have been designated and regulated to achieve specific ob-
jectives of conservation, protection and maintenance of biological diversity, as well as
associated natural and cultural resources (Dudley and Stolton 2008; Gillespie 2009).
Mexican legislation conceptualizes NPAs as areas where the original environments
have not been significantly altered by human activities, which need to be preserved
or restored and are subject to the protection regime of the General Law of Ecological
Balance and Environmental Protection (LGEEPA in Spanish) (SEMARNAT 2018).
The federal NPAs are those that are not restricted to a geopolitical limit within
the Mexican territory and are managed by the National Commission of Natural Pro-
tected Areas (CONANP 2016). Currently, Mexico has a total of 182 federal NPAs
that occupy about 13% of the national territory and are grouped into six different
categories according to their management objectives and by the type of zoning that
they may be subject to (Table 1) (Íñiguez et al. 2014; CONANP 2016). For now,
Chiapas is the Mexican state with the highest number of decreed NPAs (n = 19)
being the one that assigns one of the largest territorial extensions for its protection,
as it is located in one of the zones richest in biodiversity and natural resources from
the country (CONANP 2016).
The dung beetles of the subfamily Scarabaeinae (Coleoptera: Scarabaeidae) are a
group of insects with a wide global distribution, finding representatives on all con-
tinents (except Antarctica), but whose diversity is mainly concentrated in the tropi-
cal and subtropical regions (Scholtz et al. 2009). The ecological functions in which
these beetles are involved provide valuable ecosystem services, such as secondary
seed dispersal, nutrient cycle and biological control of pests, among others (Nich-
ols et al. 2008). Moreover, different authors have indicated that these arthropods
are organisms sensitive to structural changes in habitats caused by disturbances,
exhibiting drastic permutations in their development and distribution in the modi-
fied landscapes (Halffter and Favila 1993; Halffter and Arellano 2002; Arellano and
Halffter 2003; Reyes-Novelo et al. 2007; Otavo et al. 2013; Mannu et al. 2018).
 Dung beetles in protected areas of Chiapas, Mexico 221

Table 1. Categories and main characteristics of the Mexican Natural Protected Areas, including their
representativeness in Chiapas.

Categories Mexico Chiapas Characteristics

N Extension in ha n Extension in ha (%)
Flora and Fauna 40 6,996,864.1 4 24,980.7 (0.36) Its focus is towards the species conservation. The
Protection Area objective is to conserve the habitats where wild flora and
fauna live, develop and evolve.
Natural Resources 8 4,503,345.2 2 198,551.5 (4.41) Areas dedicated to the preservation and protection of soils,
Protected Area watersheds and natural resources of forestlands. It includes
protection areas of national water bodies, especially when
they are used to supply human populations.
Natural Monument 5 16,269.1 2 6,978.7 (42.90) Specific sites that contain natural elements with an
exceptional value of aesthetic, historical or scientific type.
Extractive type exploitation is banned.
National Park 67 16,220,099.3 3 29,583.4 (0.18) They are sites with ecosystems that have mainly scenic
beauty, historical, scientific, educational and recreational
value, that preserve special flora and fauna and that
present, above all, aptitude for tourism development.
Biosphere Reserve 44 62,952,750.5 7 932,095.8 (1.48) They are established in places that represent the diversity
of the country’s ecosystems. Representativeness is also
taken into account in terms of biological diversity and the
presence of endemic, threatened or endangered species.
Sanctuary 18 150,193.3 1 212.5 (0.14) They stand out for maintaining a high species richness or
species of restricted distribution in delimited sites. This
includes ravines, relicts, caves, cenotes, caletas and other
specific geographical units
Total 182 90,839,521.5 19 1,192,402.6 (1.3)

In order to understand the links between ecological functions and ecosystem

services they offer, some authors have proposed the subfamily Scarabaeinae as a fo-
cus group for applied research in biodiversity conservation (Spector 2006; Nichols
and Gardner 2011), categorizing it as a bioindicator that allows adequate monitoring
of the impact of anthropic alterations in tropical forests (Halffter and Favila 1993;
Favila and Halffter 1997; Spector 2006; Nichols et al. 2007). Despite the bioindicator
potential offered by this group of insects, their study in the Mexican protected areas
has been underestimated and, unlike other taxa (e.g. mammals and birds), they are
not considered within their management and conservation programs. This work
aims to provide an overview of the distribution of the Scarabaeinae species in the
federal NPAs of the state of Chiapas in order to create a reference point for future
biodiversity projects and their monitoring in these territories.

Materials and methods

Data source

Published studies on dung beetles species occurring in the federal NPAs of Chiapas
(see Table 2) were checked in the academic databases Google Scholar (www.scholar.
google.com), SciELO (www.scielo.org), Web of Science (www.isiwebofknowledge.
com) and Scopus (www.scopus.com). This search was performed using commonly
222 Gibrán Sánchez-Hernández et al.

Table 2. Characteristics of the 19 federal Natural Protected Areas decreed in Chiapas1.

Categories Name Acronym Year of decree Extension (ha) Main vegetation types*
Flora and Fauna Protected Area Agua Azul APFFAA 1980 2,580 TRF
Chan-Kin APFFCK 1992 12,184.98 TRF, MRF, SV, HV
Metzabok APFFM 1998 3,841.47 TRF, ECF, OF, SV
Nahá APFFN 1998 3,368.36 TRF, MRF, ECF
Natural Resources Protected Area La Frailescana APRNF 1997 177,546.17 TDF, TRF, MRF
Villa Allende APRNVA 1939 21,005.27 TDF, ECF, MRF, OF
Natural Monument Yaxchilán MNY 1992 2,621.25 TRF
Bonampak MNB 1992 4,357.42 TRF, MRF, ECF
National Park Cañón del Sumidero PNCS 1980 21,789.42 TDF, MRF, XV, SV
Lagunas de Montebello PNLM 1959 6,022 OF, ECF, SV
Palenque PNP 1981 1,772 TRF, G
Biosphere Reserve Lacan-Tun REBILA 1992 61,873.96 TRF, HV
Selva El Ocote REBISO 1982 101,288.15 TRF, MRF, SV
El Triunfo REBITRI 1990 119,177.29 ECF, TRF
La Encrucijada REBIEN 1995 144,868.16 M, MRF, TDF, CD
La Sepultura REBISE 1995 167,309.86 OF, PF, OPF, MRF, SV
Montes Azules REBIMA 1978 331,200 TRF, MRF, POF, ECF
Volcán Tacaná REBIVTA 2003 6,378.37 ECF, MRF
Sanctuary Playa de Puerto Arista SPPA 1986 212.48 CD, M, HV, TDF
TRF: tropical rainforest; MRF: mountain rainforest; TDF: tropical deciduous forest; ECF: evergreen cloud forest; PF: pine forest;
POF: pine-oak forest; OPF: oak-pine forest; SV: secondary vegetation; XV: xerophytic vegetation; HV: hydrophilic vegetation; M:
mangrove; CD: coastal dunes; G: grassland. 1CONANP (2016). *According Breedlove (1981).

used keywords to name the species of the subfamily Scarabaeinae, as well as terms
related to the designations of the NPAs of Chiapas and any possible combination
between them (and equivalent terms in Spanish): “dung beetles”, “Scarabaeinae”, co-
prophagous”, “necrophilous”, “copronecrophagous”, “Chiapas”, “National Park”, “Bio-
sphere Reserve”, “protected area”, “rain forest”, “cloud forest”, “deciduous forest”, “La-
candona rainforest”. Subsequently, a manual search of publications that potentially
contained data on dung beetles was carried out to avoid the exclusion of information
not contained in the academic databases (i.e. printed papers not available online),
but bypassing literature that does not conform adequately to the bibliographic con-
trol standards (e.g. thesis or technical reports). According to the studies approach,
the selected publications were classified into three general topics: 1) Taxonomic
(works containing supra-specific monographic reviews and description of new spe-
cies), 2) ecological/faunistic (systematic sampling with lists of species and analysis
of assemblages of a specific region or location) and, 3) geographical distribution
(works that include geographic range extension data). In addition, records were ob-
tained from the Global Biodiversity Information Facility database (GBIF 2019).

Institutional acronyms
The records obtained from the GBIF database come from the following entomologi-
cal collections:

CACH Colección Entomológica, Facultad de Ciencias Agronómicas, Uni-

versidad Autónoma de Chiapas, Chiapas, México;
 Dung beetles in protected areas of Chiapas, Mexico 223

CADR Colección Alfonso Díaz Rojas, Xalapa, Veracruz, México;

CEUA Colección Entomológica Universidad de Alicante, Alicante, España;
CDNG Colección Darío Navarrete Gutiérrez, San Cristóbal de Las Casas,
Chiapas, México;
CMNEN Canadian Museum of Nature Insect Collection, Ontario, Canada;
CNCI Canadian National Collection of Insects, Ontario, Canada;
CNIABM Colección Nacional de Insectos Dr. Alfredo Barrera Marín, México;
CNIN Colección Nacional de Insectos, Universidad Nacional Autónoma de
México, Ciudad de México, México;
CZRN Colección Entomológica, Instituto de Historia Natural y Ecología,
Chiapas, México;
ECO-SC-E Colección Entomológica, El Colegio de la Frontera Sur, San Cristóbal
de Las Casas, Chiapas, México;
ECO-TAP-E Colección Entomológica, El Colegio de la Frontera Sur, Tapachula,
Chiapas, México;
ERCVC Colección Eduardo Rafael Chamé Vázquez, Tapachula, Chiapas, México;
FVMC Fernando Zagury Vaz de Mello Collection, Cuiabá, Brazil;
GHAC Colección Gonzalo Halffter, Xalapa, Veracruz, México;
IAvH-E Instituto de Investigación de Recursos Biológicos Alexander von
Humboldt, Bogotá, Colombia;
IEXA Colección Entomológica Instituto de Ecología, Xalapa, Veracruz,
México;
MXAL Colección Miguel Ángel Morón, Xalapa, Veracruz, México;
SEMC Snow Entomological Museum Collection, University of Kansas, Kan-
sas, United States of America;
SMCC Scott McCleve Collection, Arizona, United States of America;
TAMU Texas A&M University Insect Collection, Texas, United States of
America;
UAIC University of Arizona Insect Collection, Arizona, United States of
America.

The list of species obtained was reviewed and updated according to the supra-
generic designation proposed by Bouchard et al. (2011) and although there are 11
recognized tribes, only seven are found in Mexico. Supra-specific revisions of the
genera Canthon (Rivera-Cervantes and Halffter 1999), Coprophanaeus (Edmonds
and Zídek 2010), Deltochilum (Génier 2012; González-Alvarado and Vaz-de-Mello
2014; Silva et al. 2015), Dichotomius (López-Guerrero 2005), Martinezidium (Vaz-
de-Mello 2008) and Phanaeus (Edmonds and Zídek 2012), were also taken into
account because they include changes of status for several species on the list. Some
species were omitted from the list and those records were considered erroneous or
corresponded to incorrect geographic records (see discussion). Finally, a review of
the red list of threatened species of the International Union for the Conservation of
Nature (IUCN 2018) was carried out to include the status in which the species on
the list could be considered.
224 Gibrán Sánchez-Hernández et al.

Data analysis
We use simple linear regressions to determine the influence of the number of pub-
lications in each NPA and its area size (has) with the number of species that each
one recorded. This analysis was performed in the R software (R Core Team 2019)
and using the ggplot2 package (Wickham 2020). To determine any similarities in
the species composition between NPAs, a cluster analysis was performed using the
unweighted pair group method (UPGMA), calculated with the Simpson index in
the software PAST v.3.26 (Hammer et al. 2001). To avoid bias due to faunistic dis-
proportion and aggregation by inclusion, NPAs with a record equal to or less than
five species were omitted from the similarity analysis.

Results

A total of 112 species and seven subspecies belonging to 23 genera, seven tribes
and four subtribes of the subfamily Scarabaeinae were found (Table 3). Tribe Del-
tochilini included the largest number of genera and species (six genera, 27 spp),
followed by Ateuchini at the generic level (five genera) and Onthophagini for their
number of species (25 spp). Sisyphini is the least representative tribe with only one
species. Onthophagus and Canthon are the most diversified genera, with 24 and 15
species, respectively, which together represent 34.82% of the total species, while
eight genera are represented by only one species (Fig. 1).
A total of 47 publications provided records of 104 species, of which 48.9%
(n = 23) corresponded to taxonomic studies, 31.9% (n = 15) were ecological/faunis-
tic works and only 19.2% (n = 9) presented geographic distribution data. For its
part, the GBIF database presented records that corresponded to 94 species. Canthon
indigaceus chevrolati (Harold, 1868), Eurysternus plebejus Harold, 1880, Onthopha-
gus championi Bates, 1887, O. corrosus (Bates, 1887), O. guatemalensis Bates, 1887,
O. marginicollis Harold, 1880, O. nasicornis Harold, 1869 and O. sharpi Harold,
1875, were not registered in any of the publications, so they were exclusive records
from this database (Table 3).
Of the 19 NPAs analyzed, 16 presented records of Scarabaeinae (84.2%), ex-
cept APFFAA, APFFCK and REBILA (Fig. 2). The species reported showed a sig-
nificant relation with the number of publications that registered them in each NPA
(R2 = 0.80, F = 56.47, P = 0.0001, Fig. 3A) but not with the area size of each one of
them (R2 = 0.069, F = 1.039, P = 0.325, Fig. 3B). REBIMA and REBISO highlighted
for presenting the largest number of registered species, both with 61, while APFFM,
REBIEN and SPPA presented records of only one species (Fig. 4). At least 20 taxa
(species and subspecies) have been described from organisms collected in ten of the
NPAs studied. According to the IUCN red list of threatened species, 13 species are
found in two low-risk categories, 12 in the least concern category and only one as
near threatened (Table 3).
A high specificity of species was found for the NPAs, with 33 species (29.5%)
registered in a protected area alone: REBIMA (n = 7), REBISO (n = 6), APRNVA
 Dung beetles in protected areas of Chiapas, Mexico 225

Table 3. List of the dung beetle species registered in the Natural Protected Areas of Chiapas, Mexico.

Species NPAs Resources

Ateuchini, Ateuchina
Ateuchus candezei (Harold, 1868) PNLM, PNP, Kohlmann 1984, 1997, 2000; Morón et al. 1985; Navarrete and
REBIMA Halffter 2008a; Delgado et al. 2012; Sánchez-de-Jesús et al.
2016; Santos-Heredia et al. 2018; GBIF 2019

Ateuchus chrysopyge (Bates, 1887) PNLM, REBIMA, Kohlmann 2000; Navarrete and Halffter 2008a, b; Sánchez-de-
REBISO Jesús et al. 2016; GBIF 2019
1
Ateuchus guatemalensis (Bates, 1887) REBIVTA Kohlmann 2000
Ateuchus illaesum (Harold, 1868) PNLM, REBIMA, Kohlmann 1984; Coutiño et al. 2005; Santos-Heredia et al.
REBIVTA 2018; GBIF 2019
*Ateuchus laetitiae Kohlmann, 1981 REBIMA Kohlmann 1981, 1984
*Ateuchus perezvelai Kohlmann, 2000 REBISO Gómez et al. 2017; Sánchez-Hernández et al. 2018
Ateuchus rodriguezi (Preudhomme de REBISO, REBIVTA, Kohlmann 1984, 1997; Arellano et al. 2008, 2009, 2013; Cancino-
Borre, 1886) APRNVA López et al. 2014; Sánchez-Hernández et al. 2018; GBIF 2019
Bdelyropsis bowditchi Paulian, 1939 REBIMA, MNB, Navarrete and Halffter 2008a; Sánchez-de-Jesús et al. 2016;
MNY Santos-Heredia et al. 2018
*2Bdelyropsis newtoni Howden, 1971 PNP Howden 1971
Uroxys boneti Pereira & Halffter, 1961 MNB, PNP, Halffter et al. 1992; Delgado and Kohlmann 2007; GBIF 2019
REBIMA, REBISO
*Uroxys deavilai Delgado & Kohlmann, PNCS, REBISO, Delgado and Kohlmann 2007; Arellano et al. 2008, 2009, 2013;
2007 APRNVA Sánchez-Hernández et al. 2018; GBIF 2019
Uroxys microcularis Howden & Young, MNB, MNY, Delgado and Kohlmann 2007; Navarrete and Halffter 2008a;
1981 REBIMA, REBISO Sánchez-de-Jesús et al. 2016; Gómez et al. 2017; Sánchez-
Hernández et al. 2018; Santos-Heredia et al. 2018; GBIF 2019
Uroxys micros Bates, 1887 PNP, REBIMA, Delgado and Kohlmann 2007; Sánchez-de-Jesús et al. 2016;
MNY GBIF 2019
Uroxys platypyga Howden & Young, 1981 MNB, REBIMA Delgado and Kohlmann 2007; Navarrete and Halffter 2008a,
b; Sánchez-de-Jesús et al. 2016; Santos-Heredia et al. 2018;
GBIF 2019
*Uroxys tacanensis Delgado & Kohlmann, REBIVTA Delgado and Kohlmann 2007
2007
Ateuchini, Scatimina
*Martinezidium maya (Vaz-de-Mello, PNCS, APRNVA Vaz-de-Mello et al. 2004; Vaz-de-Mello 2008; Arellano et al.
Halffter & Halffter, 2004) 2009, 2013; GBIF 2019
Scatimus ovatus Harold, 1862 MNB, PNLM, Génier and Kohlmann 2003, Arellano et al. 2008; Navarrete
PNCS, REBIMA, and Halffter 2008a; Arellano et al. 2009, 2013; Sánchez-de-
REBISE, REBISO, Jesús et al. 2016; Gómez et al. 2017; Sánchez-Hernández et al.
APRNVA 2018; Santos-Heredia et al. 2018; GBIF 2019
Coprini
Canthidium ardens Bates, 1887 REBIMA, REBIVTA, Arellano et al. 2008; Navarrete and Halffter 2008a; Cancino-
APRNVA López et al. 2014; Sánchez-de-Jesús et al. 2016; Santos-Heredia
et al. 2018; GBIF 2019
Canthidium centrale Boucomont, 1928 MNB, REBIMA, Palacios-Ríos et al. 1990; Morón et al. 1985; Kohlmann and
REBISE, REBISO, Solís 2006; Navarrete and Halffter 2008; Blas and Gómez 2009;
MNY Sánchez-de-Jesús et al. 2016; Sánchez-Hernández et al. 2018;
Santos-Heredia et al. 2018; GBIF 2019
Canthidium laetum Harold, 1867 APRNVA Arellano et al. 2009, 2013; GBIF 2019
*Canthidium moroni Kohlmann & Solís, APFFN, REBIMA, Kohlmann and Solís 2006; Gómez et al. 2017
2006 REBISO
*Canthidium pseudoperceptibile MNB, APFFN, Kohlmann and Solís 2006; Sánchez-Hernández et al. 2018;
Kohlmann & Solís, 2006 APRNVA, REBIMA, GBIF 2019
REBISO
*Canthidium pseudopuncticolle Solís & REBISO Kohlmann and Solís 2006; Sánchez-Hernández et al. 2018;
Kohlmann, 2004 GBIF 2019
Canthidium vespertinum Howden & REBIMA Navarrete and Halffter 2008a; Sánchez-de-Jesús et al. 2016;
Young, 1981 GBIF 2019
*Copris costaricensis dolichocerus REBIVTA Matthews 1961; Coutiño et al. 2005; Cancino-López et al. 2014;
Matthews, 1961 GBIF 2019
226 Gibrán Sánchez-Hernández et al.

Species NPAs Resources

Copris incertus Say, 1835 APRNVA, Arellano et al. 2009, 2013; GBIF 2019
REBIVTA, PNCS
Copris laeviceps Harold, 1862 PNP, REBIMA, Morón et al. 1985; Palacios-Ríos et al.1990; Arellano et al.
REBISO, MNY, 2008; Navarrete and Halffter 2008a; Arellano et al. 2009, 2013;
APRNVA, PNCS Sánchez-de-Jesús et al. 2016; Gómez et al. 2017; Darling and
Génier 2018; Sánchez-Hernández et al. 2018; Santos-Heredia et
al. 2018; GBIF 2019
Copris lugubris Boheman, 1858 APRNF, PNLM, Morón et al. 1985; Palacios-Ríos et al.1990; Arellano et al. 2008,
REBISO, REBISE, 2009; Blas and Gómez 2009; Navarrete and Halffter 2008a;
APFFN, REBIMA, Arellano et al. 2013; Sánchez-de-Jesús et al. 2016; Darling and
REBITRI, MNY, Génier 2018; Santos-Heredia et al. 2018; GBIF 2019
REBIVTA, APRNVA
*1Copris matthewsi matthewsi Delgado & PNLM Delgado and Kohlmann 2001
Kohlmann, 2001
*1Copris matthewsi pacificus Delgado & REBITRI, REBIVTA Delgado and Kohlmann 2001; Coutiño et al. 2005; Cancino-
Kohlmann, 2001 López et al. 2014
Dichotomius amplicollis (Harold, 1869) PNLM, PNP, PNCS, Morón et al. 1985; Halffter et al. 1992; Arellano et al. 2008,
REBIMA, REBISO, 2009; Blas and Gómez 2009; Navarrete and Halffter 2008a;
APRNF, REBITRI, Arellano et al. 2013; Sánchez-de-Jesús et al. 2016; Sánchez-
APRNVA, Hernández et al. 2018; Santos-Heredia et al. 2018; GBIF 2019
Dichotomius annae Kohlmann & Solís, REBIMA, REBISE, Coutiño et al. 2005; Navarrete and Halffter 2008; Sánchez-de-
1997 REBITRI, REBIVTA Jesús et al. 2016; GBIF 2019
Dichotomius colonicus Say, 1835 PNLM, PNCS, PNP, Arellano et al. 2008, 2009; Delgado et al. 2012; Arellano et al.
REBIMA, APRNF, 2013, Gómez et al. 2017; GBIF 2019
REBISE, APRNVA,
REBISO, REBITRI,
REBIVTA
1
Dichotomius maya Peraza & Deloya, 2006 REBISO Sánchez-Hernández et al. 2019
Dichotomius satanas Harold, 1867 APRNVA, PNLM, Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992;
PNP, REBIMA, Navarrete and Halffter 2008; Blas and Gómez 2009; Delgado
REBISO, MNY et al. 2012; Sánchez-de-Jesús et al. 2016; Santos-Heredia et al.
2018; GBIF 2019
1
Ontherus azteca Harold, 1869 REBIMA, REBISO Génier 1996; Navarrete and Halffter 2008a; GBIF 2019
*Ontherus mexicanus Harold, 1868 PNLM, REBISO Génier 1996; Gómez et al. 2017
Deltochilini
Agamopus lampros Bates, 1887 APRNVA Arellano et al. 2008, 2009, 2013
Canthon angustatus Harold, 1867 PNP, REBIMA Chamé-Vázquez and Gómez 2005; Navarrete and Halffter
2008a; Halffter and Halffter 2009; Sánchez-de-Jesús et al. 2016;
Santos-Heredia et al. 2018; GBIF 2019
Canthon championi Bates, 1887 REBISO, REBITRI Blas and Gómez 2009; GBIF 2019
Canthon cyanellus LeConte, 1859 REBISO, PNCS, Morón et al. 1985; Palacios-Ríos et al.1990; Halffter et al. 1992;
PNP, REBIMA, Arellano et al. 2008, 2009; Navarrete and Halffter 2008a; Blas
REBIVTA, MNY, and Gómez 2009; Arellano et al. 2013; Sánchez-de-Jesús et al.
APRNVA 2016; Sánchez-Hernández et al. 2018; GBIF 2019
Canthon delgadoi Rivera-Cervantes & APRNVA Arellano et al. 2008, 2009; Halffter and Halffter 2009; Arellano
Halffter, 1999 et al. 2013; GBIF 2019
Canthon euryscelis Bates, 1887 MNB, PNP, MNY, Morón et al. 1985; Rivera-Cervantes and Halffter 1999;
REBISO, REBIMA Navarrete and Halffter 2008a; Sánchez-de-Jesús et al. 2016;
Santos-Heredia et al. 2018; GBIF 2019
Canthon femoralis (Chevrolat, 1834) PNCS, REBIMA, Morón et al. 1985; Palacios-Ríos et al. 1990; Rivera-Cervantes
PNP, REBISO, and Halffter 1999; Navarrete and Halffter 2008a; Arellano et al.
REBISE, MNY, 2009, 2013; Sánchez-de-Jesús et al. 2016; Sánchez-Hernández
APRNVA et al. 2018; Santos-Heredia et al. 2018; GBIF 2019
Canthon humectus incisus Robinson, 1948 PNLM, APRNVA, Delgado et al. 2012; GBIF 2019
PNCS
Canthon humectus sayi Robinson, 1948 APRNVA, PNCS Arellano et al. 2008, 2009, 2013; GBIF 2019
1
Canthon indigaceus chevrolati Harold, PNCS, REBIEN GBIF 2019
1868
 Dung beetles in protected areas of Chiapas, Mexico 227

Species NPAs Resources

1
Canthon indigaceus chiapas Robinson, APRNVA, PNCS, Arellano et al. 2008, 2009; Blas and Gómez 2009; Arellano et al.
1948 PNLM, REBISE, 2013; GBIF 2019
REBISO
Canthon leechi (Martínez, Halffter & PNCS, PNLM, PNP, Halffter et al. 1992; Rivera-Cervantes and Halffter 1999;
Halffter, 1964) REBIMA, REBISE, Navarrete and Halffter 2008; Sánchez-Hernández et al. 2018;
REBISO GBIF 2019
1
Canthon lituratus (Germar, 1813) REBIMA Navarrete and Halffter 2008a, b; GBIF 2019
*Canthon lucreciae Halffter & Halffter, 2009 APRNVA Halffter and Halffter 2009; Arellano et al. 2013
Canthon meridionalis (Martínez, Halffter REBISO Gómez et al. 2017
& Halffter, 1964)
Canthon morsei Howden, 1966 MNY, PNP, Palacios-Ríos et al. 1990; Navarrete and Halffter 2008a; Halffter
REBIMA, REBISO and Halffter 2009; Sánchez-de-Jesús et al. 2016; GBIF 2019
1
Canthon subhyalinus subhyalinus Harold, MNB, MNY, PNP, Palacios-Ríos et al. 1990; Halffter et al. 1992; Rivera-Cervantes
1867 REBIMA, REBISO and Halffter 1999; Navarrete and Halffter 2008a; Sánchez-de-
Jesús et al. 2016; Santos-Heredia et al. 2018; GBIF 2019
Canthon vazquezae (Martínez, Halffter & MNB, MNY, PNCS, Palacios-Ríos et al. 1990; Rivera-Cervantes and Halffter
Halffter, 1964) PNP, REBIMA, 1999; Arellano et al. 2008; Blas and Gómez 2009; Sánchez-
REBISE, REBISO, Hernández et al. 2018; GBIF 2019
APRNVA
*Cryptocanthon montebello Cook, 2002 PNLM Cook 2002; GBIF 2019
Deltochilum acropyge Bates, 1887 REBISO, MNY Cano 1998; Blas and Gómez 2009; GBIF 2019
*Deltochilum carrilloi González-Alvarado REBISO, REBIMA, González-Alvarado and Vaz-de-Mello 2014
& Vaz-de-Mello, 2014 APRNVA
Deltochilum densepunctatum Balthasar, REBISO González-Alvarado and Vaz-de-Mello 2014
1939
Deltochilum lobipes Bates, 1887 REBIMA, APRNVA Arellano et al. 2008, 2009; Navarrete and Halffter 2008a;
Arellano et al. 2013; Sánchez-de-Jesús et al. 2016; Santos-
Heredia et al. 2018; GBIF 2019
Deltochilum mexicanum Burmeister, 1848 PNLM, REBISO, Coutiño et al. 2005; Blas and Gómez 2009; Delgado et al. 2012;
REBITRI, REBIVTA Cancino-López et al. 2014; Sánchez-Hernández et al. 2018;
GBIF 2019
Deltochilum pseudoparile Paulian, 1938 PNP, REBIMA, Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992;
REBISO, MNB, Navarrete and Halffter 2008a; Blas and Gómez 2009; Sánchez-
MNY, APRNVA de-Jesús et al. 2016; Sánchez-Hernández et al. 2018; Santos-
Heredia et al. 2018; GBIF 2019
Deltochilum scabriusculum Bates, 1887 PNCS, PNLM, PNP, Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992;
REBIMA, REBISE, Arellano et al. 2008, 2009; Navarrete and Halffter 2008a; Génier
REBISO, REBITRI, 2012; Arellano et al. 2013; Sánchez-de-Jesús et al. 2016; Sánchez-
MNY, APRNVA Hernández et al. 2018; Santos-Heredia et al. 2018; GBIF 2019
Deltochilum sublaeve Bates, 1887 PNLM, PNP, MNY, Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992;
APRNVA, REBIMA, Navarrete and Halffter 2008; Arellano et al. 2009; Blas and
REBISO, REBITRI, Gómez 2009; Arellano et al. 2013; Cancino-López et al. 2014;
REBIVTA González-Alvarado and Vaz-de-Mello 2014; Sánchez-de-Jesús
et al. 2016; Sánchez-Hernández et al. 2018; Santos-Heredia et
al. 2018; GBIF 2019
Megathoposoma candezei Harold, 1873 MNY, PNP, Morón et al. 1985; Halffter et al. 1992; Navarrete and Halffter
REBIMA 2008a; Sánchez-de-Jesús et al. 2016; Santos-Heredia et al. 2018;
GBIF 2019
Pseudocanthon perplexus (LeConte, 1847) APRNVA, PNCS, Arellano et al. 2008; GBIF 2019
PNP
Oniticellini, Eurysternina
Eurysternus angustulus Harold, 1869 APFFM, MNB, PNP, Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992;
REBIMA, REBISO, Navarrete and Halffter 2008a; Génier 2009; Sánchez-de-Jesús
MNY et al. 2016; Gómez et al. 2017; Sánchez-Hernández et al. 2018;
Santos-Heredia et al. 2018; GBIF 2019
Eurysternus caribaeus Herbst, 1789 MNB, PNLM, PNP, Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992;
REBIMA, REBISO, Navarrete and Halffter 2008a; Blas and Gómez 2009; Génier
MNY 2009; Delgado et al. 2012; Sánchez-Hernández et al. 2018;
Santos-Heredia et al. 2018; GBIF 2019
228 Gibrán Sánchez-Hernández et al.

Species NPAs Resources

Eurysternus foedus Guérin, 1844 REBIMA, REBISO, Morón et al. 1985; Navarrete and Halffter 2008a; Génier 2009;
Sánchez-de-Jesús et al. 2016; Sánchez-Hernández et al. 2018;
Santos-Heredia et al. 2018; GBIF 2019
Eurysternus magnus Castelnau, 1840 APRNF, PNLM, Coutiño et al. 2005; Génier 2009; Sánchez-de-Jesús et al. 2016;
PNCS, PNP, Sánchez-Hernández et al. 2018; GBIF 2019
REBIMA, REBISE,
REBISO, REBIVTA
*Eurysternus maya Génier, 2009 MNB Génier 2009
Eurysternus mexicanus Harold, 1869 MNB, PNLM, PNP, Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992;
REBIMA, REBISO, Navarrete and Halffter 2008a; Arellano et al. 2009; Génier
APRNVA, MNY 2009; Arellano et al. 2013; Sánchez-de-Jesús et al. 2016; Santos-
Heredia et al. 2018; GBIF 2019
Eurysternus plebejus Harold, 1880 REBIMA GBIF 2019
Eurysternus velutinus Bates, 1887 REBIMA Morón et al. 1985
Oniticellini, Oniticellina
#
Euoniticellus intermedius (Reiche, 1849) REBISE, REBISO, Morales et al. 2004; Coutiño et al. 2005; Arellano et al. 2008,
REBITRI, APRNVA, 2009, 2013; GBIF 2019
REBIVTA
Onthophagini
#
Digitonthophagus gazella (Fabricius, REBISO, REBITRI, Morales et al. 2004; Arellano et al. 2008; GBIF 2019
1757) SPPA, PNP,
APRNVA, APRNF
Onthophagus acuminatus Harold, 1880 REBIMA, APRNVA Delgado 1997; Navarrete and Halffter 2008a; Arellano et al.
2009, 2013; Sánchez-de-Jesús et al. 2016; Santos-Heredia et al.
2018; GBIF 2019
Onthophagus anthracinus Harold, 1873 REBISO, REBIVTA Coutiño et al. 2005; Cancino-López et al. 2014; Gómez et al.
2017; GBIF 2019
Onthophagus batesi Howden & PNLM, PNCS, Palacios-Ríos et al. 1990; Halffter et al. 1992; Arellano et
Cartwright, 1963 REBIMA, REBISE, al. 2008; Navarrete and Halffter 2008a; Delgado et al. 2012;
REBISO, REBITRI, Arellano et al. 2013; Sánchez-de-Jesús et al. 2016; Gómez et al.
PNP, MNY, 2017; Santos-Heredia et al. 2018; GBIF 2019
APRNVA
Onthophagus belorhinus Bates, 1887 REBISE GBIF 2019
1
Onthophagus carpophilus Pereira & APFFN, REBIMA, Navarrete and Halffter 2008a; Sánchez-de-Jesús et al. 2016;
Halffter, 1961 REBISO, MNY, PNP Sánchez-Hernández et al. 2018; Santos-Heredia et al. 2018;
GBIF 2019
Onthophagus championi Bates 1887 REBISE GBIF 2019
*Onthophagus chiapanecus Zunino & REBISE, REBITRI Zunino and Halffter 1988; GBIF 2019
Halffter, 1988
Onthophagus coscineus Bates, 1887 REBIMA Delgado 1997; Navarrete and Halffter 2008a; Sánchez-de-Jesús
et al. 2016 Santos-Heredia et al. 2018; GBIF 2019
Onthophagus corrosus Bates, 1887 PNP GBIF 2019
Onthophagus crinitus Harold, 1869 PNP, REBIMA, Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992;
REBISO, MNY, Arellano et al. 2008; Navarrete and Halffter 2008a; Blas and
APRNVA Gómez 2009; Arellano et al. 2013; Sánchez-de-Jesús et al. 2016;
Sánchez-Hernández et al. 2018; Santos-Heredia et al. 2018;
GBIF 2019
Onthophagus cyanellus Bates, 1887 PNLM, REBISE, Coutiño et al. 2005; Delgado et al. 2012; Cancino-López et al.
REBITRI, REBIVTA 2014; GBIF 2019
Onthophagus cyclographus Bates, 1887 PNLM, REBIMA, Navarrete and Halffter 2008a; Sánchez-Hernández et al. 2018
REBISO
Onthophagus guatemalensis Bates, 1887 REBISE, REBITRI, GBIF 2019
PNP
Onthophagus igualensis Bates, 1887 APRNVA, PNCS, Arellano et al. 2008, 2013; GBIF 2019
PNP, REBISE,
REBITRI
Onthophagus incensus Say, 1835 REBIMA, REBISO, Coutiño et al. 2005; Navarrete and Halffter 2008a; Cancino-
REBIVTA, PNP, López et al. 2014; Gómez et al. 2017; Sánchez-Hernández et al.
MNY 2018; GBIF 2019
 Dung beetles in protected areas of Chiapas, Mexico 229

Species NPAs Resources

Onthophagus landolti Harold, 1880 PNP, REBISO, Halffter et al. 1992; Kohlmann and Solís 2001; Arellano et al.
APRNVA 2009, 2013; Gómez et al. 2017; Sánchez-Hernández et al. 2018;
GBIF 2019
Onthophagus longimanus Bates, 1887 REBISO Sánchez-Hernández et al. 2017; Sánchez-Hernández et al. 2018
Onthophagus marginicollis Harold, 1880 PNP GBIF 2019
*Onthophagus maya Zunino, 1981 REBIMA, REBISE, Morón et al. 1985; Palacios-Ríos et al. 1990; Blas and Gómez
REBISO, MNY, PNP 2009; Navarrete and Halffter 2008a; Sánchez-de-Jesús et al.
2016; Sánchez-Hernández et al. 2018; Santos-Heredia et al.
2018; GBIF 2019
Onthophagus nasicornis Harold, 1869 REBIMA, PNP GBIF 2019
Onthophagus rhinolophus Harold, 1869 PNLM, PNP, Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992;
REBIMA, REBISO, Navarrete and Halffter 2008a; Blas and Gómez 2009; Delgado
MNY et al. 2012; Sánchez-de-Jesús et al. 2016; Sánchez-Hernández et
al. 2018; Santos-Heredia et al. 2018; GBIF 2019
Onthophagus sharpi Harold, 1875 PNP GBIF 2019
Onthophagus violetae Zunino & Halffter, APRNVA, APFFN Arellano et al. 2009, 2013; GBIF 2019
1997
Onthophagus yucatanus Delgado, Peraza REBIMA, REBISO Navarrete and Halffter 2008a, b; Sánchez-de-Jesús et al. 2016;
& Deloya, 2006 Gómez et al. 2017; Sánchez-Hernández et al. 2018; Santos-
Heredia et al. 2018
Phanaeini
1
Coprophanaeus corythus Harold, 1863 MNB, PNP, Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992;
REBIVTA, REBIMA, Coutiño et al. 2005; Arellano et al. 2008, 2009; Navarrete and
REBISO, MNY, Halffter 2008a; Blas and Gómez 2009; Edmonds and Zidek
APRNVA 2010; Arellano et al. 2013; Cancino-López et al. 2014; Sánchez-
de-Jesús et al. 2016; Sánchez-Hernández et al. 2018; Santos-
Heredia et al. 2018; GBIF 2019
Coprophanaeus gilli Arnaud, 1997 MNB, REBIMA, Navarrete and Halffter 2008a, Edmonds and Zidek 2010;
REBISO, PNP Sánchez-Hernández et al. 2018; GBIF 2019
Coprophanaeus pluto Harold, 1863 REBITRI Edmonds and Zidek 2010; GBIF 2019
Phanaeus amethystinus Harold, 1863 MNY, PNLM, Edmonds 1994; GBIF 2019
REBISE, REBITRI
Phanaeus demon Castelnau, 1840 REBISE, APRNVA, Edmonds 1994; Arellano et al. 2009, 2013; GBIF 2019
PNCS
Phanaeus endymion Harold, 1863 MNB, PNCS, Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992;
PNLM, PNP, Edmonds 1994; Navarrete and Halffter 2008a; Blas and Gómez
REBIMA, REBISO, 2009; Arellano et al. 2013; Cancino-López et al. 2014; Sánchez-
REBIVTA, MNY, de-Jesús et al. 2016; Sánchez-Hernández et al. 2018; Santos-
APRNVA Heredia et al. 2018; GBIF 2019
Phanaeus guatemalensis Harold, 1871 REBIVTA Coutiño et al. 2005; Cancino-López et al. 2014; GBIF 2019
Phanaeus melampus Harold, 1863 REBIMA Navarrete and Edmonds 2006; Navarrete and Halffter 2008a;
GBIF 2019
Phanaeus pilatei Harold, 1863 MNY Palacios-Ríos et al. 1990
1
Phanaeus pyrois Bates, 1887 REBISO, REBIVTA, Delgado 1997; Arellano et al. 2008, 2009; Blas and Gómez
APRNVA 2009; GBIF 2019
Phanaeus sallei Harold, 186 MNB, MNY, PNP, Morón et al. 1985; Halffter et al. 1992; Edmonds 1994;
PNLM REBIMA, Navarrete and Halffter 2008a; Palacios-Ríos et al. 1990;
REBISO Sánchez-de-Jesús et al. 2016; Sánchez-Hernández et al. 2018;
Santos-Heredia et al. 2018; GBIF 2019
1
Phanaeus tridens Laporte-Castelnau, REBISE, REBISO, Edmonds 1994; Arellano et al. 2009, 2013; GBIF 2019
1840 REBITRI, PNCS,
APRNVA
Phanaeus wagneri Harold, 1873 PNLM, PNCS, Edmonds 1994; Arellano et al. 2008, 2009, 2013
APRNVA
Sulcophanaeus chryseicollis (Harold, 1863) MNB, REBIMA, Halffter et al. 1992; Edmonds 2000; Navarrete and Halffter
REBISO, PNP 2008a; Sánchez-de-Jesús et al. 2016; GBIF 2019
Sisyphini
Sisyphus mexicanus Harold, 1863 REBITRI Gómez and Chamé-Vázquez 2003; GBIF 2019
*Species/subspecies described from organisms collected in Natural Protected Areas of Chiapas. #Invasive species. 1Least concern
and 2Near threatened in the IUCN Red List.
230 Gibrán Sánchez-Hernández et al.

Figure 1. Number of species registered by genus in the Natural Protected Areas of Chiapas.

Figure 2. Natural Protected Areas of Chiapas grouped into five categories according to the number of
species they register. See acronym in Table 2.
 Dung beetles in protected areas of Chiapas, Mexico 231

Figure 3. Simple linear regression analysis between the (A) species recorded and the publications that
register them; and (B) with the area size of each natural protected areas.

Figure 4. Number of species and genera of Scarabaeinae registered by Natural Protected Area in Chiapas.

(n = 4), PNP (n = 4), REBIVTA (n = 4), PNLM (n = 2), REBISE (n = 2), REBITRI
(n = 2), MNB (n = 1) and MNY (n = 1). The similarity analysis indicated the forma-
tion of three large groups of reserves with faunistic similarities (Fig. 5). One of them
is formed by the reserves in the Sierra Madre de Chiapas, where montane forests
predominate (REBISE and REBITRI) with approximately 87% similarity; another
group corresponding to tropical rain forests consisted of five reserves (MNB, MNY,
PNP, REBIMA and REBISO) with about 73% similarity; and the last was composed
of two NPAs of deciduous forests (APRNVA and PNCS) with 60% similarity. PNLM
232 Gibrán Sánchez-Hernández et al.

Figure 5. Faunistic similarity analysis of dung beetles between the Natural Protected Areas of Chia-
pas. Only NPAs with more than five registered species were included.

was more related to the rain forests and shared 50% of its fauna with this group, but
with typical elements of montane forests that separated it from the group; while
REBIVTA was isolated from the rest of the reserves, sharing a low percentage of its
fauna with all of them.

Discussion
Biodiversity of Scarabaeinae in the NPAs of Chiapas

The 112 species reported in the federal natural protected areas correspond to 91% of
the Scarabaeinae fauna of Chiapas and 38.1% of the 294 species estimated for Mex-
ico (Sánchez-Hernández and Gómez 2018; Sánchez-Hernández et al. 2019). While
the numbers reported here are high, knowledge about dung beetles in Chiapas is far
from complete. Of the total publications revised, there were few studies that corre-
spond to inventory works with systematic sampling (32.6%), restricted to only sev-
en of the protected areas (APRNVA, MNY, REBIMA, REBISO, REBIVTA, PNLM
and PNP). The NPAs with the highest number of registered species (i.e. REBIMA
and REBISO) were, in the same way, the ones that present the greatest number of
studies, while most of them lacked studies that extensively analyze the Scarabaeinae
communities. This greatly prevents the study of several basic and applied aspects
 Dung beetles in protected areas of Chiapas, Mexico 233

of dung beetles, from diversity and distribution to conservation. The above also
shows evidence that a greater sampling effort focused on the least studied reserves
would increase the possibility of discovering unregistered or described species and,
thereby, broadening the knowledge of the dung beetle diversity in Chiapas, regard-
less of the area size of the NPAs.
REBIVTA, the reserve with the lowest faunistic affinity in the study, is located
in an area with Central American influence that emerged during the volcanism
in the Pliocene (Halffter 2003). This reserve is located at a point of confluence of
three tectonic plates (Cocos, North American and Caribbean) and is limited by the
trench of Central America and the Motagua-Polochic fault system (García-Palomo
et al. 2006). Cano et al. (2018) consider its geology as a biogeographic barrier that
separates the Passalidae (Coleoptera) faunas between Central America (including
the Tacaná volcano) and southeastern Mexico. Similarly, they recognize that the
Motagua-Cuilco dry valleys system and the Motozintla-Comaltitlán suture zones
represent barriers involved in beetles vicariance processes, including other genera
of Passalidae (Schuster 1993; Schuster et al. 2003), Scarabaeidae (Micó et al. 2006),
and Carabidae (Sokolov and Kavanaugh 2014). This would explain the isolation of
the fauna found in the REBIVTA against the other Chiapas reserves, because its
function as a biogeographic barrier that prevents Central American elements from
crossing northwards on the Pacific slope.
PNP, REBISO, MNY, REBIMA and MNB, formed a faunistic complex of rain
forests located on the gulf slope with a high percentage of similarity (above 70%).
They became a group of reserves clearly different from the other group formed by
the interaction of two areas (PNCS and APRNVA) characterized by dry forests.
Both NPAs groups are made up of fauna with neotropical affinity that is distributed
over the biogeographic province of the Gulf of Mexico (Morrone 2006), but which
diverge by the type of vegetation they present. Finally, the PNLM is a reserve that
presents transition characteristics between the rain forests (Gulf of Mexico prov-
ince) and the temperate forests (Chiapas province) formed by species with Central
American and central Mexico origin (Delgado 2011), thereby separating it from the
Gulf of Mexico NPAs groups.

Species with doubtful distribution in Chiapas

We consider that seven species cited by some of the reviewed works do not have a
presence in Chiapas, or that their distribution needs to be confirmed in some of the
reserves studied. The reports of Dichotomius centralis (Harold, 1869) in the works of
Morón et al. (1985), Palacios-Ríos et al. (1990) and Halffter et al. (1992) correspond
to D. amplicollis (Harold, 1869). The overlap area of these species is in Guatemala
and D. centralis is likely to be marginally on the Pacific slope, however its presence
in Chiapas has not been confirmed (López-Guerrero 2005).
Gomez et al. (2017) reported to Dichotomius carolinus (Linnaeus, 1767) and
Dichotomius amicitiae Kohlmann & Solís, 1997, but none of these species has been
234 Gibrán Sánchez-Hernández et al.

corroborated in Mexico. Dichotomius carolinus is distributed exclusively in the

United States and the individuals rather correspond to D. colonicus, a species with
which it relates and is widely distributed in Mexico. On the other hand, D. amicitiae
is a species whose distribution is restricted to Costa Rica and Panama (Kohlmann
and Solís 1997), hence this record was confused with D. annae, a closely related
Mexican species (Peraza and Deloya 2006).
Similarly, Morón et al. (1985) cited Onthophagus nasicornis Harold, 1869 but
the species is only known in central Mexico and, this record has not been corrobo-
rated in Chiapas. Onthophagus nitidior Bates, 1887 is distributed in the low decidu-
ous and subdeciduous forests of the Mexican Central Pacific slope (Hernández and
Navarrete-Heredia 2018), so that, the report by Palacios-Ríos et al. (1990) on the
Gulf of Mexico slope, is possibly incorrect record and corresponds to other species
of the same group (hirculus species group) reported in Chiapas.
We also consider that Onthophagus rhinophyllus Harold, 1868, a species that is
distributed only in Venezuela and Colombia (Delgado et al. 2006), constitutes an er-
roneous record of Halffter et al. (1992). Onthophagus atrosericeus Boucomont, 1932,
is another species erroneously cited in Mexico. The distribution of this species is
restricted to mountains of elevation greater than 1,700 m in Costa Rica and Panama
(Kohlmann and Solís 2001), while the record of Halffter et al. (1992) is in a locality
at ~100 m altitude, approximately 1,000 km from its nearest record in Costa Rica.

Monitoring and conservation

Biodiversity monitoring in natural protected areas represents an integral component
to assess its performance and provide the information necessary for effective man-
agement (Halffter et al. 2015). In this sense, Schuster et al. (2000) mention that the
use of a group that meets the bioindicator requirements can save time and money in
conservation strategies and, at the same time, give objective and reliable criteria for
the prioritization of areas, especially when the change in land use is accelerated and
the need for conservation is urgent. One of the key reasons to conserve and monitor
invertebrates in these areas is to ensure adequate protection of rare and threatened
species and communities. Furthermore, many of them are appropriate and highly
effective and informative indicators of other elements of biodiversity, ecosystem
health and associated threats (McGeoch et al. 2011; Gerlach et al. 2013).
Due to the great variety of ecological functions in which they intervene (Nich-
ols et al. 2008), their ability to respond in the short term to forest fragmentation
(Nichols et al. 2007), its developed correlation and direct dependence on the pres-
ence of mammals in the ecosystem (Nichols et al. 2009; Bogoni et al. 2016; Mannu
et al. 2018), the inclusion of the subfamily Scarabaeinae in these types of studies has
been widely justified. They are well defined from a taxonomic and functional view-
point, and methods for their sampling has been standardized (Spector 2006; Nichols
and Gardner 2011). In addition, the analysis of their communities allows different
and more detailed results which can be obtained in relation to works based only
 Dung beetles in protected areas of Chiapas, Mexico 235

on the study of vertebrates and plants (Kohlmann et al. 2007). So that, inventories
and monitoring of Scarabaeinae communities can be useful during several stages of
NPAs management, but statistically rigorous estimates of species richness, informa-
tion on their spatial and temporal distribution are required, or their design should
target to threatened and rare species or to identify possible indicator and/or inva-
sive species (Engelbretch 2010). However, despite its characteristics as a bioindicator
group, in Mexico the dung beetles are not included among the priority groups with-
in the monitoring programs that support the management of NPAs, underestimat-
ing their results compared to those that produce studies on vertebrates and plants.
On the other hand, conservation efforts through NPAs would be much more rel-
evant and effective when they are linked at a landscape or ecosystem scale (Mocte-
zuma et al. 2018), because the resulting connectivity is essential for the biological
diversity of the areas included, as it allows genetic and energy exchange through
a greater geographical extent (Roy et al. 2010). For Scarabaeinae, these ecosystem
complexes can promote the dispersion and survival of populations of certain com-
mon species in conserved areas of the region and, at the same time, maintain the
optimal conditions for species with a restricted range of distribution. For instance,
although the 13 species indicated on the IUCN red list of threatened species (see
Table 3) do not meet the criteria to be considered in some type of immediate risk,
most of these species present isolated populations in habitats with a high degree of
vulnerability and reduced geographical range, some of them, known only from the
material used for its description. Due to these characteristics, these species could be
considered rare and indicators of conservation, which makes it necessary to con-
sider adaptation measures to guarantee the survival of their populations. However,
at present, there are no conservation strategies for any of them (IUCN 2018). Like-
wise, it would be important to establish strategies for monitoring the populations
of D. gazella and E. intermedius, two invasive alien species widely distributed in
Mexico that have been reported in several NPAs of Chiapas and that have prob-
ably been established in other contiguous reserves, since they have a high dispersal
capacity, and can negatively affect the abundance of most native species, favoring
the local extinction of species with similar nesting behavior (Montes de Oca and
Halffter 1998; Filho et al. 2018).
In Chiapas, the ecosystem-scale conservation approach through corridors that
link protected areas has recently emerged. An example of this is the “Complejo Sel-
va Zoque of Natural Protected Areas”, whose objective is to enable the connectivity
and conservation of biodiversity between five protected areas, three federal NPAs
(REBISO, APRNVA and PNCS) and two state-protected areas (La Pera and Cerro
Meyapac) (RAC 2015). This can be taken as a reference to establish connectivity
strategies that allow the genetic flow between NPAs from other regions with similar
characteristics. For example, in the Lacandona rainforest, a region that has been
seriously affected by the accelerated change in land use, mainly due to the rapid
expansion of oil palm crops, replacing large areas of forest in Chiapas (Castellanos-
Navarrete and Jansen 2018). Unlike other tree crops, oil palm is a particularly poor
236 Gibrán Sánchez-Hernández et al.

substitute for either primary or degraded forests and especially damaging to biodi-
versity (Fitzherbert et al. 2008), including the functional (Edwards et al. 2014) and
taxonomic diversity of dung beetles (Gray et al. 2014; Harada et al. 2020).
Data presented in this work can be used as a reference to monitor dung bee-
tle communities in the NPAs of Chiapas, both to conduct research in areas that
have not been investigated and to continue monitoring in the NPAs explored,
and thus analyze the dynamics of the communities over time. These studies can
help to understand their response to ecosystem alterations, since indirectly re-
ducing the beetles’ diversity through different factors of anthropic origin puts
ecosystems at risk and promotes the loss of biodiversity. These changes will have
significant negative impacts on the functional and ecological services that this
insect group provide. Therefore, it is recommended that groups of arthropods
such as the Scarabaeinae should be included in the previous justifying studies for
the designation or establishment of NPAs and in turn considered in the biological
monitoring programs of these reserves since they meet the characteristics of an
efficient bioindicator group.

Acknowledgements

We are grateful to Bridget Davis for reviewing the English grammar of the manu-
script. We also thank the two reviewers and subject editor for their useful comments
and suggestions to the manuscript. Finally, we want to recognize the work that the
Comisión Nacional de Áreas Naturales Protegidas (CONANP) does to conserve the
natural heritage of Mexico.

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