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Research Article
Current status of dung beetles (Coleoptera, Scarabaeidae, Scarabaeinae) diversity and conservation in Natural Protected Areas in Chiapas (Mexico)
expand article infoGibrán Sánchez-Hernández, Benigno Gómez, Eduardo Rafael Chamé-Vázquez§, Rolando A. Dávila-Sánchez|, M. Edivaldo Rodríguez-López, Leonardo Delgado
‡ Conservación de la Biodiversidad, San Cristóbal de Las Casas, Mexico
§ Ecología de Artrópodos y Manejo de Plagas, Tapachula, Mexico
| Ingeniería Ambiental, Managua, Nicaragua
¶ Instituto de Ecología AC, Xalapa, Mexico
Open Access

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 territorial 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 low percentage of them correspond to studies with systematic samplings and most of the species reported 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 communities 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 objectives 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 Protected 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).

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 Protection Area 40 6,996,864.1 4 24,980.7 (0.36) Its focus is towards the species conservation. The objective is to conserve the habitats where wild flora and fauna live, develop and evolve.
Natural Resources Protected Area 8 4,503,345.2 2 198,551.5 (4.41) Areas dedicated to the preservation and protection of soils, 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)

The dung beetles of the subfamily Scarabaeinae (Coleoptera: Scarabaeidae) are a group of insects with a wide global distribution, finding representatives on all continents (except Antarctica), but whose diversity is mainly concentrated in the tropical 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 (Nichols 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 modified 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).

In order to understand the links between ecological functions and ecosystem services they offer, some authors have proposed the subfamily Scarabaeinae as a focus 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 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”, coprophagous”, “necrophilous”, “copronecrophagous”, “Chiapas”, “National Park”, “Biosphere Reserve”, “protected area”, “rain forest”, “cloud forest”, “deciduous forest”, “Lacandona 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 control 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 species), 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 obtained from the Global Biodiversity Information Facility database (GBIF 2019).

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

Institutional acronyms

The records obtained from the GBIF database come from the following entomological collections:

CACH Colección Entomológica, Facultad de Ciencias Agronómicas, Universidad Autónoma de Chiapas, Chiapas, México;

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, Kansas, 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.

Data analysis

We use simple linear regressions to determine the influence of the number of publications 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 disproportion 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 Deltochilini 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).

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, REBIMA Kohlmann 1984, 1997, 2000; Morón et al. 1985; Navarrete and 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, REBISO Kohlmann 2000; Navarrete and Halffter 2008a, b; Sánchez-de-Jesús et al. 2016; GBIF 2019
1 Ateuchus guatemalensis (Bates, 1887) REBIVTA Kohlmann 2000
Ateuchus illaesum (Harold, 1868) PNLM, REBIMA, REBIVTA Kohlmann 1984; Coutiño et al. 2005; Santos-Heredia et al. 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 Borre, 1886) REBISO, REBIVTA, APRNVA Kohlmann 1984, 1997; Arellano et al. 2008, 2009, 2013; Cancino-López et al. 2014; Sánchez-Hernández et al. 2018; GBIF 2019
Bdelyropsis bowditchi Paulian, 1939 REBIMA, MNB, MNY Navarrete and Halffter 2008a; Sánchez-de-Jesús et al. 2016; Santos-Heredia et al. 2018
*2Bdelyropsis newtoni Howden, 1971 PNP Howden 1971
Uroxys boneti Pereira & Halffter, 1961 MNB, PNP, REBIMA, REBISO Halffter et al. 1992; Delgado and Kohlmann 2007; GBIF 2019
*Uroxys deavilai Delgado & Kohlmann, 2007 PNCS, REBISO, APRNVA Delgado and Kohlmann 2007; Arellano et al. 2008, 2009, 2013; Sánchez-Hernández et al. 2018; GBIF 2019
Uroxys microcularis Howden & Young, 1981 MNB, MNY, REBIMA, REBISO Delgado and Kohlmann 2007; Navarrete and Halffter 2008a; 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, MNY Delgado and Kohlmann 2007; Sánchez-de-Jesús et al. 2016; 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, 2007 REBIVTA Delgado and Kohlmann 2007
Ateuchini, Scatimina
*Martinezidium maya (Vaz-de-Mello, Halffter & Halffter, 2004) PNCS, APRNVA Vaz-de-Mello et al. 2004; Vaz-de-Mello 2008; Arellano et al. 2009, 2013; GBIF 2019
Scatimus ovatus Harold, 1862 MNB, PNLM, PNCS, REBIMA, REBISE, REBISO, APRNVA Génier and Kohlmann 2003, Arellano et al. 2008; Navarrete and Halffter 2008a; Arellano et al. 2009, 2013; Sánchez-de-Jesús et al. 2016; Gómez et al. 2017; Sánchez-Hernández et al. 2018; Santos-Heredia et al. 2018; GBIF 2019
Coprini
Canthidium ardens Bates, 1887 REBIMA, REBIVTA, APRNVA Arellano et al. 2008; Navarrete and Halffter 2008a; Cancino-López et al. 2014; Sánchez-de-Jesús et al. 2016; Santos-Heredia et al. 2018; GBIF 2019
Canthidium centrale Boucomont, 1928 MNB, REBIMA, REBISE, REBISO, MNY Palacios-Ríos et al. 1990; Morón et al. 1985; Kohlmann and Solís 2006; Navarrete and Halffter 2008; Blas and Gómez 2009; 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, 2006 APFFN, REBIMA, REBISO Kohlmann and Solís 2006; Gómez et al. 2017
*Canthidium pseudoperceptibile Kohlmann & Solís, 2006 MNB, APFFN, APRNVA, REBIMA, REBISO Kohlmann and Solís 2006; Sánchez-Hernández et al. 2018; GBIF 2019
*Canthidium pseudopuncticolle Solís & Kohlmann, 2004 REBISO Kohlmann and Solís 2006; Sánchez-Hernández et al. 2018; GBIF 2019
Canthidium vespertinum Howden & Young, 1981 REBIMA Navarrete and Halffter 2008a; Sánchez-de-Jesús et al. 2016; GBIF 2019
*Copris costaricensis dolichocerus Matthews, 1961 REBIVTA Matthews 1961; Coutiño et al. 2005; Cancino-López et al. 2014; GBIF 2019
Copris incertus Say, 1835 APRNVA, REBIVTA, PNCS Arellano et al. 2009, 2013; GBIF 2019
Copris laeviceps Harold, 1862 PNP, REBIMA, REBISO, MNY, APRNVA, PNCS Morón et al. 1985; Palacios-Ríos et al.1990; Arellano et al. 2008; Navarrete and Halffter 2008a; Arellano et al. 2009, 2013; 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, REBISO, REBISE, APFFN, REBIMA, REBITRI, MNY, REBIVTA, APRNVA Morón et al. 1985; Palacios-Ríos et al.1990; Arellano et al. 2008, 2009; Blas and Gómez 2009; Navarrete and Halffter 2008a; Arellano et al. 2013; Sánchez-de-Jesús et al. 2016; Darling and Génier 2018; Santos-Heredia et al. 2018; GBIF 2019
*1Copris matthewsi matthewsi Delgado & Kohlmann, 2001 PNLM Delgado and Kohlmann 2001
*1Copris matthewsi pacificus Delgado & Kohlmann, 2001 REBITRI, REBIVTA Delgado and Kohlmann 2001; Coutiño et al. 2005; Cancino-López et al. 2014
Dichotomius amplicollis (Harold, 1869) PNLM, PNP, PNCS, REBIMA, REBISO, APRNF, REBITRI, APRNVA, Morón et al. 1985; Halffter et al. 1992; Arellano et al. 2008, 2009; Blas and Gómez 2009; Navarrete and Halffter 2008a; Arellano et al. 2013; Sánchez-de-Jesús et al. 2016; Sánchez-Hernández et al. 2018; Santos-Heredia et al. 2018; GBIF 2019
Dichotomius annae Kohlmann & Solís, 1997 REBIMA, REBISE, REBITRI, REBIVTA Coutiño et al. 2005; Navarrete and Halffter 2008; Sánchez-de-Jesús et al. 2016; GBIF 2019
Dichotomius colonicus Say, 1835 PNLM, PNCS, PNP, REBIMA, APRNF, REBISE, APRNVA, REBISO, REBITRI, REBIVTA Arellano et al. 2008, 2009; Delgado et al. 2012; Arellano et al. 2013, Gómez et al. 2017; GBIF 2019
1Dichotomius maya Peraza & Deloya, 2006 REBISO Sánchez-Hernández et al. 2019
Dichotomius satanas Harold, 1867 APRNVA, PNLM, PNP, REBIMA, REBISO, MNY Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992; Navarrete and Halffter 2008; Blas and Gómez 2009; Delgado 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, PNP, REBIMA, REBIVTA, MNY, APRNVA Morón et al. 1985; Palacios-Ríos et al.1990; Halffter et al. 1992; Arellano et al. 2008, 2009; Navarrete and Halffter 2008a; Blas and Gómez 2009; Arellano et al. 2013; Sánchez-de-Jesús et al. 2016; Sánchez-Hernández et al. 2018; GBIF 2019
Canthon delgadoi Rivera-Cervantes & Halffter, 1999 APRNVA Arellano et al. 2008, 2009; Halffter and Halffter 2009; Arellano et al. 2013; GBIF 2019
Canthon euryscelis Bates, 1887 MNB, PNP, MNY, REBISO, REBIMA Morón et al. 1985; Rivera-Cervantes and Halffter 1999; Navarrete and Halffter 2008a; Sánchez-de-Jesús et al. 2016; Santos-Heredia et al. 2018; GBIF 2019
Canthon femoralis (Chevrolat, 1834) PNCS, REBIMA, PNP, REBISO, REBISE, MNY, APRNVA Morón et al. 1985; Palacios-Ríos et al. 1990; Rivera-Cervantes and Halffter 1999; Navarrete and Halffter 2008a; Arellano et al. 2009, 2013; Sánchez-de-Jesús et al. 2016; Sánchez-Hernández et al. 2018; Santos-Heredia et al. 2018; GBIF 2019
Canthon humectus incisus Robinson, 1948 PNLM, APRNVA, PNCS Delgado et al. 2012; GBIF 2019
Canthon humectus sayi Robinson, 1948 APRNVA, PNCS Arellano et al. 2008, 2009, 2013; GBIF 2019
1Canthon indigaceus chevrolati Harold, 1868 PNCS, REBIEN GBIF 2019
1Canthon indigaceus chiapas Robinson, 1948 APRNVA, PNCS, PNLM, REBISE, REBISO Arellano et al. 2008, 2009; Blas and Gómez 2009; Arellano et al. 2013; GBIF 2019
Canthon leechi (Martínez, Halffter & Halffter, 1964) PNCS, PNLM, PNP, REBIMA, REBISE, REBISO Halffter et al. 1992; Rivera-Cervantes and Halffter 1999; Navarrete and Halffter 2008; Sánchez-Hernández et al. 2018; GBIF 2019
1Canthon 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 & Halffter, 1964) REBISO Gómez et al. 2017
Canthon morsei Howden, 1966 MNY, PNP, REBIMA, REBISO Palacios-Ríos et al. 1990; Navarrete and Halffter 2008a; Halffter and Halffter 2009; Sánchez-de-Jesús et al. 2016; GBIF 2019
1Canthon subhyalinus subhyalinus Harold, 1867 MNB, MNY, PNP, REBIMA, REBISO Palacios-Ríos et al. 1990; Halffter et al. 1992; Rivera-Cervantes and Halffter 1999; Navarrete and Halffter 2008a; Sánchez-de-Jesús et al. 2016; Santos-Heredia et al. 2018; GBIF 2019
Canthon vazquezae (Martínez, Halffter & Halffter, 1964) MNB, MNY, PNCS, PNP, REBIMA, REBISE, REBISO, APRNVA Palacios-Ríos et al. 1990; Rivera-Cervantes and Halffter 1999; Arellano et al. 2008; Blas and Gómez 2009; Sánchez-Hernández et al. 2018; GBIF 2019
*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 & Vaz-de-Mello, 2014 REBISO, REBIMA, APRNVA González-Alvarado and Vaz-de-Mello 2014
Deltochilum densepunctatum Balthasar, 1939 REBISO González-Alvarado and Vaz-de-Mello 2014
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, REBITRI, REBIVTA Coutiño et al. 2005; Blas and Gómez 2009; Delgado et al. 2012; Cancino-López et al. 2014; Sánchez-Hernández et al. 2018; GBIF 2019
Deltochilum pseudoparile Paulian, 1938 PNP, REBIMA, REBISO, MNB, MNY, APRNVA Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992; Navarrete and Halffter 2008a; Blas and Gómez 2009; Sánchez-de-Jesús et al. 2016; Sánchez-Hernández et al. 2018; Santos-Heredia et al. 2018; GBIF 2019
Deltochilum scabriusculum Bates, 1887 PNCS, PNLM, PNP, REBIMA, REBISE, REBISO, REBITRI, MNY, APRNVA Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992; Arellano et al. 2008, 2009; Navarrete and Halffter 2008a; Génier 2012; Arellano et al. 2013; Sánchez-de-Jesús et al. 2016; Sánchez-Hernández et al. 2018; Santos-Heredia et al. 2018; GBIF 2019
Deltochilum sublaeve Bates, 1887 PNLM, PNP, MNY, APRNVA, REBIMA, REBISO, REBITRI, REBIVTA Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992; Navarrete and Halffter 2008; Arellano et al. 2009; Blas and Gómez 2009; Arellano et al. 2013; Cancino-López et al. 2014; 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, REBIMA Morón et al. 1985; Halffter et al. 1992; Navarrete and Halffter 2008a; Sánchez-de-Jesús et al. 2016; Santos-Heredia et al. 2018; GBIF 2019
Pseudocanthon perplexus (LeConte, 1847) APRNVA, PNCS, PNP Arellano et al. 2008; GBIF 2019
Oniticellini, Eurysternina
Eurysternus angustulus Harold, 1869 APFFM, MNB, PNP, REBIMA, REBISO, MNY Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992; Navarrete and Halffter 2008a; Génier 2009; Sánchez-de-Jesús 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, REBIMA, REBISO, MNY Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992; Navarrete and Halffter 2008a; Blas and Gómez 2009; Génier 2009; Delgado et al. 2012; Sánchez-Hernández et al. 2018; Santos-Heredia et al. 2018; GBIF 2019
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, PNCS, PNP, REBIMA, REBISE, REBISO, REBIVTA Coutiño et al. 2005; Génier 2009; Sánchez-de-Jesús et al. 2016; Sánchez-Hernández et al. 2018; GBIF 2019
*Eurysternus maya Génier, 2009 MNB Génier 2009
Eurysternus mexicanus Harold, 1869 MNB, PNLM, PNP, REBIMA, REBISO, APRNVA, MNY Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992; Navarrete and Halffter 2008a; Arellano et al. 2009; Génier 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, REBITRI, APRNVA, REBIVTA Morales et al. 2004; Coutiño et al. 2005; Arellano et al. 2008, 2009, 2013; GBIF 2019
Onthophagini
#Digitonthophagus gazella (Fabricius, 1757) REBISO, REBITRI, SPPA, PNP, APRNVA, APRNF Morales et al. 2004; Arellano et al. 2008; GBIF 2019
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 & Cartwright, 1963 PNLM, PNCS, REBIMA, REBISE, REBISO, REBITRI, PNP, MNY, APRNVA Palacios-Ríos et al. 1990; Halffter et al. 1992; Arellano et al. 2008; Navarrete and Halffter 2008a; Delgado et al. 2012; Arellano et al. 2013; Sánchez-de-Jesús et al. 2016; Gómez et al. 2017; Santos-Heredia et al. 2018; GBIF 2019
Onthophagus belorhinus Bates, 1887 REBISE GBIF 2019
1 Onthophagus carpophilus Pereira & Halffter, 1961 APFFN, REBIMA, REBISO, MNY, PNP Navarrete and Halffter 2008a; Sánchez-de-Jesús et al. 2016; Sánchez-Hernández et al. 2018; Santos-Heredia et al. 2018; GBIF 2019
Onthophagus championi Bates 1887 REBISE GBIF 2019
*Onthophagus chiapanecus Zunino & Halffter, 1988 REBISE, REBITRI Zunino and Halffter 1988; GBIF 2019
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, REBISO, MNY, APRNVA Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992; Arellano et al. 2008; Navarrete and Halffter 2008a; Blas and 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, REBITRI, REBIVTA Coutiño et al. 2005; Delgado et al. 2012; Cancino-López et al. 2014; GBIF 2019
Onthophagus cyclographus Bates, 1887 PNLM, REBIMA, REBISO Navarrete and Halffter 2008a; Sánchez-Hernández et al. 2018
Onthophagus guatemalensis Bates, 1887 REBISE, REBITRI, PNP GBIF 2019
Onthophagus igualensis Bates, 1887 APRNVA, PNCS, PNP, REBISE, REBITRI Arellano et al. 2008, 2013; GBIF 2019
Onthophagus incensus Say, 1835 REBIMA, REBISO, REBIVTA, PNP, MNY Coutiño et al. 2005; Navarrete and Halffter 2008a; Cancino-López et al. 2014; Gómez et al. 2017; Sánchez-Hernández et al. 2018; GBIF 2019
Onthophagus landolti Harold, 1880 PNP, REBISO, APRNVA Halffter et al. 1992; Kohlmann and Solís 2001; Arellano et al. 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, REBISO, MNY, PNP Morón et al. 1985; Palacios-Ríos et al. 1990; Blas and Gómez 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, REBIMA, REBISO, MNY Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992; Navarrete and Halffter 2008a; Blas and Gómez 2009; Delgado 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, 1997 APRNVA, APFFN Arellano et al. 2009, 2013; GBIF 2019
Onthophagus yucatanus Delgado, Peraza & Deloya, 2006 REBIMA, REBISO Navarrete and Halffter 2008a, b; Sánchez-de-Jesús et al. 2016; Gómez et al. 2017; Sánchez-Hernández et al. 2018; Santos-Heredia et al. 2018
Phanaeini
1Coprophanaeus corythus Harold, 1863 MNB, PNP, REBIVTA, REBIMA, REBISO, MNY, APRNVA Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992; Coutiño et al. 2005; Arellano et al. 2008, 2009; Navarrete and Halffter 2008a; Blas and Gómez 2009; Edmonds and Zidek 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, REBISO, PNP Navarrete and Halffter 2008a, Edmonds and Zidek 2010; Sánchez-Hernández et al. 2018; GBIF 2019
Coprophanaeus pluto Harold, 1863 REBITRI Edmonds and Zidek 2010; GBIF 2019
Phanaeus amethystinus Harold, 1863 MNY, PNLM, REBISE, REBITRI Edmonds 1994; GBIF 2019
Phanaeus demon Castelnau, 1840 REBISE, APRNVA, PNCS Edmonds 1994; Arellano et al. 2009, 2013; GBIF 2019
Phanaeus endymion Harold, 1863 MNB, PNCS, PNLM, PNP, REBIMA, REBISO, REBIVTA, MNY, APRNVA Morón et al. 1985; Palacios-Ríos et al. 1990; Halffter et al. 1992; Edmonds 1994; Navarrete and Halffter 2008a; Blas and Gómez 2009; 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
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
1Phanaeus pyrois Bates, 1887 REBISO, REBIVTA, APRNVA Delgado 1997; Arellano et al. 2008, 2009; Blas and Gómez 2009; GBIF 2019
Phanaeus sallei Harold, 186 MNB, MNY, PNP, PNLM REBIMA, REBISO Morón et al. 1985; Halffter et al. 1992; Edmonds 1994; Navarrete and Halffter 2008a; Palacios-Ríos et al. 1990; Sánchez-de-Jesús et al. 2016; Sánchez-Hernández et al. 2018; Santos-Heredia et al. 2018; GBIF 2019
1Phanaeus tridens Laporte-Castelnau, 1840 REBISE, REBISO, REBITRI, PNCS, APRNVA Edmonds 1994; Arellano et al. 2009, 2013; GBIF 2019
Phanaeus wagneri Harold, 1873 PNLM, PNCS, APRNVA Edmonds 1994; Arellano et al. 2008, 2009, 2013
Sulcophanaeus chryseicollis (Harold, 1863) MNB, REBIMA, REBISO, PNP Halffter et al. 1992; Edmonds 2000; Navarrete and Halffter 2008a; Sánchez-de-Jesús et al. 2016; GBIF 2019
Sisyphini
Sisyphus mexicanus Harold, 1863 REBITRI Gómez and Chamé-Vázquez 2003; GBIF 2019
Figure 1. 

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

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/faunistic 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, Onthophagus 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%), except APFFAA, APFFCK and REBILA (Fig. 2). The species reported showed a significant 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).

Figure 2. 

Natural Protected Areas of Chiapas grouped into five categories according to the number of species they register. See acronym in Table 2.

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.

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 (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 formation 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 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.

Figure 5. 

Faunistic similarity analysis of dung beetles between the Natural Protected Areas of Chiapas. Only NPAs with more than five registered species were included.

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 Mexico (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 correspond to inventory works with systematic sampling (32.6%), restricted to only seven 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 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, regardless 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 province) 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 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 corroborated in Chiapas. Onthophagus nitidior Bates, 1887 is distributed in the low deciduous 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 erroneous 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 management (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 (Nichols 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 presence 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 viewpoint, 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 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, information 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 invasive species (Engelbretch 2010). However, despite its characteristics as a bioindicator group, in Mexico the dung beetles are not included among the priority groups within the monitoring programs that support the management of NPAs, underestimating their results compared to those that produce studies on vertebrates and plants.

On the other hand, conservation efforts through NPAs would be much more relevant and effective when they are linked at a landscape or ecosystem scale (Moctezuma 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 common 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 consider adaptation measures to guarantee the survival of their populations. However, at present, there are no conservation strategies for any of them (IUCN 2018). Likewise, 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 probably 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 Selva 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 substitute for either primary or degraded forests and especially damaging to biodiversity (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 beetle 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 reducing 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 manuscript. 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.

References

  • Arellano L, Halffter G (2003) Gamma diversity: derived from and a determinant of alpha diversity and beta diversity. An analysis of three tropical landscape. Acta Zoológica Mexicana (n.s. ) 90: 27–76.
  • Arellano L, León-Cortes JL, Halffter G (2008) Response of dung beetle assemblages to landscape structure in remnant natural and modified habitats in southern Mexico. Insect Conservation and Diversity 1(4): 253–262. https://doi.org/10.1111/j.1752-4598.2008.00033.x
  • Arellano L, León-Cortes JL, Halffter G (2009) Cambios en la diversidad de escarabajos estercoleros (Coleoptera: Scarabaeinae) en un sistema silvopastoril Chiapaneco. In: Estrada EG, Equihua E, Chaires MP, Acuña JA, Padilla JR, Mendoza A (Eds) Entomología Mexicana (Vol. 8). Sociedad Mexicana de Entomología, Mexico City, 274–279.
  • Arellano L, León-Cortes JL, Halffter G, Montero J (2013) Acacia woodlots, cattle and dung beetles (Coleoptera: Scarabaeinae) in a Mexican silvopastoral landscape. Revista Mexicana de Biodiversidad 84(2): 650–660. https://doi.org/10.7550/rmb.32911
  • Bezaury-Creel J, Gutiérrez Carbonell D (2009) Áreas naturales protegidas y desarrollo social en México. In: Dirzo R, González R, March IJ (Comp.) Capital natural de México, vol. II: Estado de conservación y tendencias de cambio. CONABIO, Mexico city, 385–431.
  • Blas M, Gómez B (2009) Escarabajos (Coleoptera: Scarabaeidae). In: Riechers A, Morales JE, Hernández E (Comp.) Laguna Bélgica: Patrimonio natural e interpretación ambiental. Instituto de Historia Natural. Chiapas, 75–87.
  • Bogoni JA, Graipel ME, De Castilho PV, Fantacini FM, Kuhnen VV, Luiz MR, Maccarini TB, Marcon CB, Teixeira CSP, Tortato MA, Vaz-de-Mello FZ, Hernández MIM (2016) Contributions of the mammal community, habitat structure, and spatial distance to dung beetle community structure. Biodiversity and Conservation 25(9): 1661–1675. https://doi.org/10.1007/s10531-016-1147-1
  • Bouchard P, Bousquet Y, Davies AE, Alonso-Zarazaga MA, Lawrence JF, Lyal CHCA, Newton F, Reid CAM, Schmitt M, Ślipiński SA, Smith ABT (2011) Family-group names in Coleoptera (Insecta). ZooKeys 88: 1–972. https://doi.org/10.3897/zookeys.88.807
  • Breedlove DE (1981) Flora of Chiapas: Introduction to the flora of Chiapas. California Academy of Sciences, San Francisco, 33 pp.
  • Cancino-López RJ, Chamé-Vázquez ER, Gómez B (2014) Escarabajos necrófilos (Coleoptera: Scarabaeinae) en tres hábitats del Volcán Tacaná, Chiapas, México. Dugesiana 21(2): 135–142. https://doi.org/10.32870/dugesiana.v21i2.4152
  • Cano EB (1998) Deltochilum valgum acropyge Bates (Coleoptera: Scarabaeidae: Scarabaeinae): Habits and Distribution. Coleopterists Bulletin 52(2): 174–178. https://www.jstor.org/stable/4009382
  • Cano EB, Schuster JC, Morrone JJ (2018) Phylogenetics of Ogyges Kaup and the biogeography of Nuclear Central America (Coleoptera, Passalidae). ZooKeys 737: 81–111. https://doi.org/10.3897/zookeys.737.20741
  • Castellanos-Navarrete A, Jansen K (2018) Is oil palm expansion a challenge to agroecology? Smallholders practising industrial farming in Mexico. Journal of Agrarian Change 18(1): 132–155. https://doi.org/10.1111/joac.12195
  • Comisión Nacional de Áreas Naturales Protegidas (CONANP) (2016) Prontuario Estadístico y Geográfico de las Áreas Naturales Protegidas de México (1st Edn.). Secretaría de Medio Ambiente y Recursos Naturales, Mexico city.
  • Coutiño TA, Gómez B, López-Rojas J (2005) Lista preliminar de escarabajos copronecrófagos (Coleoptera: Scarabaeinae) en el municipio de Unión Juárez, Chiapas, México. In: Morales Moreno A, Mendoza Estrada A, Ibarra González MP, Stanford Camargo S (Eds) Entomología Mexicana (Vol. 4). Sociedad Mexicana de Entomología, Mexico City, 897–901.
  • Darling JDG, Génier F (2018) Revision of the taxonomy and distribution of the Neotropical Copris incertus species complex (Coleoptera: Scarabaeidae: Scarabaeinae). Canadian Entomologist 150(5): 539–577. https://doi.org/10.4039/tce.2018.32
  • Delgado JM (2011) Diversidad de Scarabaeoidea (Coleoptera) en los principales tipos de vegetación de Montebello, Chiapas, México. M.Sc. thesis, Chiapas, Mexico: El Colegio de la Frontera Sur. https://doi.org/10.21829/azm.2012.281825
  • Delgado JM, Castro-Ramírez AE, Morón MA, Ruiz-Montoya L (2012) Diversidad de Scarabaeoidea (Coleoptera) en las principales condiciones de hábitat de Montebello, Chiapas, México. Acta Zoológica Mexicana (n.s. ) 28(1): 185–210. https://doi.org/10.21829/azm.2012.281825
  • Delgado L (1997) Distribución estatal de la diversidad y nuevos registros de Scarabaeidae (Coleoptera) mexicanos. Folia Entomologica Mexicana 99: 37–56.
  • Delgado L, Kohlmann B (2007) Revisión de las especies del género Uroxys Westwood de México y Guatemala (Coleoptera: Scarabaeidae: Scarabaeinae). Folia Entomologica Mexicana 46(1): 1–36.
  • Dudley N, Stolton S (2008) Defining protected areas: an international conference in Almeria, Spain. IUCN, Gland, 220 pp.
  • Edmonds WD (1994) Revision of Phanaeus Macleay, a new world genus of Scarabaeinae dung beetles (Coleoptera: Scarabaeidae, Scarabaeinae). Contributions in Science 443: 1–105.
  • Edmonds WD (2000) Revision of the Neotropical dung beetle genus Sulcophanaeus (Coleoptera: Scarabaeidae: Scarabaeinae). Folia Heyrovskyana (Supplementum 6): 1–60.
  • Edwards FA, Edwards DP, Larsen TH, Benedick S, Chung A, Vun Ken C, Wilcove DS, Hamer KC (2014) Does logging and forest conversion to oil palm agriculture alter functional diversity in a biodiversity hotspot? Animal Conservation 17(2): 163–173. https://doi.org/10.1111/acv.12074
  • Filho WM, Flechtmann CAH, Godoy WAC, Bjornstad ON (2018) The impact of the introduced Digitonthophagus gazella on a native dung beetle community in Brazil during 26 years. Biological Invasions 20(4): 963–979. https://doi.org/10.1007/s10530-017-1603-1
  • Fitzherbert EB, Struebig MJ, Morel A, Danielsen F, Brühl CA, Donald PF, Phalan B (2008) How will oil palm expansion affect biodiversity? Trends in Ecology & Evolution 23(10): 538–545. https://doi.org/10.1016/j.tree.2008.06.012
  • García-Palomo A, Macías JL, Arce JL, Mora JC, Hughes S, Saucedo R, Espíndola JM, Escobar R, Layer P (2006) Geological evolution of the Tacaná Volcanic Complex, México-Guatemala. In: Rose WI, Bluth GJS, Carr MJ, Ewert JW, Patino LC, Vallance JW (Eds) Volcanic hazards in Central America. Geological Society of America, Colorado, Special Paper 412: 39–57. https://doi.org/10.1130/2006.2412(03)
  • Génier F (1996) A revision of the Neotropical genus Ontherus Erichson (Coleoptera: Scarabaeidae, Scarabaeinae). Memoirs of the Entomological Society of Canada 128(S170): 3–169. https://doi.org/10.4039/entm128170fv
  • Génier F (2009) Le Genre Eurysternus Dalman, 1824 (Scarabaeidae: Scarabaeinae: Oniticellini): Révision taxonomique et clés de détermination illustrées. Pensoft Publishers, Sofia, 430 pp.
  • Génier F (2012) A new species and notes on the subgenus Deltochilum (Deltochilum) Eschscholtz, 1822 (Coleoptera: Scarabaeidae: Scarabaeinae: Deltochilini). Zootaxa 3357(1): 25–36. https://doi.org/10.11646/zootaxa.3357.1.2
  • Génier F, Kohlmann B (2003) Revision of the Neotropical dung beetle genera Scatimus Erichson and Scatrichus gen. nov. (Coleoptera: Scarabaeidae: Scarabaeinae). Fabreries 28(2): 57–111.
  • Gerlach J, Samways M, Pryke J (2013) Terrestrial invertebrates as bioindicators: An overview of available taxonomic groups. Journal of Insect Conservation 17(4): 831–850. https://doi.org/10.1007/s10841-013-9565-9
  • Global Biodiversity Information Facility (GBIF) (2019) The Catalog of Life Partnership. www.gbif.org [accessed on 10.03.2019]
  • Gómez B, Chamé-Vázquez ER (2003) Primeros registros de Goniophileurus femoratus y Sisyphus mexicanus para Chiapas, México (Coleoptera: Scarabaeoidea). Folia Entomológica Mexicana (n.s. ) 42(1): 103–104.
  • Gómez B, Pozo C, de la Mora-Estrada LF, Domínguez MR, Rodríguez-López ME, Ruiz-Montoya L (2017) Diversidad de insectos colectados en cuatro localidades de la Reserva de la Biosfera Selva El Ocote. In: Ruiz-Montoya L, Álvarez-Gordillo G, Ramírez-Marcial N. Cruz-Salazar B (Eds) Vulnerabilidad social y biológica ante el cambio climático en la Reserva de la Biosfera Selva El Ocote. El Colegio de la Frontera Sur, Chiapas, 171–254.
  • González-Alvarado A, Vaz-de-Mello FZ (2014) Taxonomic review of the subgenus Hybomidium Shipp 1897 (Coleoptera: Scarabaeidae: Scarabaeinae: Deltochilum). Annales de la Société entomologique de France (N.S. ) 50(3–4): 431–476. https://doi.org/10.1080/00379271.2014.989178
  • Gray CL, Slade EM, Mann DJ, Lewis OT (2014) Do riparian reserves support dung beetle biodiversity and ecosystem services in oil palm‐dominated tropical landscapes? Ecology and Evolution 4(7): 1049–1060. https://doi.org/10.1002/ece3.1003
  • Halffter G (2003) Biogeografía de la entomofauna de montaña de México y América Central. In: Morrone JJ, Llorente Bousquets J (Eds) Una Perspectiva Latinoamericana de la Biogeografía. Las Prensas de Ciencias, Mexico City, 87–99.
  • Halffter G, Favila ME (1993) The Scarabaeinae (Insecta: Coleoptera) an animal group for analyzing, inventorying and monitoring biodiversity in tropical rainforest and modified landscapes. Biology International 27: 15–21.
  • Halffter G, Favila ME, Halffter V (1992) A comparative study of the structure of the scarab guild in Mexican tropical rain forest and derived ecosystems. Folia Entomologica Mexicana 84: 131–156.
  • Halffter G, Tinoco-Ojanguren C, Iñiguez-Dávalos LI, Ortega-Rubio A (2015) La investigación científica y las Áreas Naturales Protegidas en México: Una relación exitosa. In: Ortega-Rubio A, Pinkus-Rendón MJ, Espitia-Moreno IC (Eds) Las Áreas Naturales Protegidas y la investigación científica en México. Centro de Investigaciones Biológicas del Noreste, Universidad Autónoma de Yucatán, Universidad Michoacana de San Nicolas de Hidalgo, Mexico, 3–18.
  • Harada LM, Araújo IS, Overal WL, Silva FAB (2020) Comparison of dung beetle communities (Coleoptera: Scarabaeidae: Scarabaeinae) in oil palm plantations and native forest in the eastern Amazon, Brazil. Revista Brasileira de Entomologia 64(1): e2019102. https://doi.org/10.1590/1806-9665-rbent-2019-102
  • Hernández B, Navarrete-Heredia JL (2018) Annotated checklist and biogeographical affinities of Scarabaeinae beetles from Los Altos de Jalisco region, Mexico. Southwestern Entomologists 43(1): 131–149. https://doi.org/10.3958/059.043.0130
  • Íñiguez LI, Jiménez CL, Sosa J, Ortega-Rubio A (2014) Categorías de las áreas naturales protegidas en México y una propuesta para la evaluación de su efectividad. Investigacion y Ciencia 60: 65–70. https://www.redalyc.org/pdf/674/67431160008.pdf
  • Kohlmann B (1981) Nuevas especies de Ateuchus (Coleoptera: Scarabaeidae) de México. Folia Entomologica Mexicana (49): 71–92.
  • Kohlmann B (1984) Biosistemática de las especies norteamericanas de género Ateuchus (Coleoptera: Scarabaeidae: Scarabaeinae). Folia Entomologica Mexicana 60: 3–81.
  • Kohlmann B, Solís A (1997) El género Dichotomius (Coleoptera: Scarabaeidae) en Norteamérica. Giornale Italiano di Entomologia 8(47): 343–382.
  • Kohlmann B, Solís A (2001) El género Onthophagus (Coleoptera: Scarabaeidae) en Costa Rica. Giornale Italiano di Entomologia 9(49): 159–261.
  • Kohlmann B, Solís A (2006) El género Canthidium (Coleoptera: Scarabaeidae) en Norteamérica. Giornale Italiano di Entomologia 11(52): 235–295.
  • Kohlmann B, Solís A, Elle O, Soto X, Russo R (2007) Biodiversity, conservation and hotspot atlas of Costa Rica: a dung beetle perspective (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 1457(1): 1–34. https://doi.org/10.11646/zootaxa.1457.1.1
  • Mannu R, Pilia O, Fadda ML, Verdinelli L (2018) Variability of beetle assemblages in Mediterranean cork oak woodlands: Does the higher taxa approach reliably characterize a specific response to grazing? Biodiversity and Conservation 27(14): 3599–3619. https://doi.org/10.1007/s10531-018-1616-9
  • McGeoch MA, Sithole H, Samways MJ, Simaika JP, Pryke JS, Picker M, Uys C, Armstrong AJ, Dippenaar-Schoeman AS, Engelbrecht IA, Hamer M (2011) Conservation and monitoring of invertebrates in terrestrial protected areas. Koedoe 53(2): a1000. https://doi.org/10.4102/koedoe.v53i2.1000
  • Moctezuma V, Halffter G, Arriaga-Jiménez A (2018) Archipelago reserves, a new option to protect montane entomofauna and beta-diverse ecosystems. Revista Mexicana de Biodiversidad 89(3): 927–937. https://doi.org/10.22201/ib.20078706e.2018.3.2446
  • Montes de Oca E, Halffter G (1998) Invasion of Mexico by two dung beetles previously introduced into the United States. Studies on Neotropical Fauna and Environment 33(1): 37–45. https://doi.org/10.1076/snfe.33.1.37.2174
  • Morales CJ, Ruiz R, Delgado L (2004) Primer registro de Euoniticellus intermedius (Reiche, 1849) y datos nuevos de distribución de Digitonthophagus gazella (Fabricius, 1787) (Coleoptera: Scarabaeidae) e Hybosorus illigeri Reiche, 1853 (Coleoptera: Hybosoridae) para el estado de Chiapas. Dugesiana 11(2): 21–23.
  • Morón MA, Villalobos JA, Deloya C (1985) Fauna de coleopteros lamelicornios de Boca de Chajul, Chiapas, México. Folia Entomologica Mexicana 66: 57–118.
  • Morrone JJ (2006) Biogeographic areas and transition zones of Latin America and the Caribbean islands based on panbiogeographic and cladistic analyses of the entomofauna. Annual Review of Entomology 51(1): 467–494. https://doi.org/10.1146/annurev.ento.50.071803.130447
  • Navarrete DA, Edmonds WD (2006) New field record for the rare dung beetle, Phanaeus melampus Harold (Coleoptera: Scarabaeidae: Scarabaeinae. Coleopterists Bulletin 60(1): 67–68. https://doi.org/10.1649/839.1
  • Navarrete DA, Halffter G (2008a) Dung beetle (Coleoptera: Scarabaeidae: Scarabaeinae) diversity in continuous forest, forest fragments and cattle pastures in a landscape of Chiapas, Mexico: the effects of anthropogenic changes. Biodiversity and Conservation 17(4): 2869–2898. https://doi.org/10.1007/s10531-008-9402-8
  • Navarrete DA, Halffter G (2008b) Nuevos registros de escarabajos copro-necrófagos (Coleoptera: Scarabaeidae: Scarabaeinae) para México y Chiapas. Acta Zoológica Mexicana (n.s. ) 24(1): 247–250. https://doi.org/10.21829/azm.2008.241637
  • Nichols E, Gardner TA (2011) Dung beetles as a candidate study taxon in applied biodiversity conservation research. In: Simmons LW, Ridsdill-Smith TJ (Eds) Ecology and Evolution of Dung Beetles. Wiley-Blackwell, Oxford, 267–339. https://doi.org/10.1002/9781444342000.ch13
  • Nichols E, Larsen T, Spector S, Davis AL, Escobar F, Favila M, Vulenic K (2007) Global dung beetle response to tropical forest modification and fragmentation: A quantitative literature review and meta-analysis. Biological Conservation 137(1): 1–19. https://doi.org/10.1016/j.biocon.2007.01.023
  • Nichols E, Spector S, Louzada J, Larsen T, Amezquita S, Favila ME (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biological Conservation 141(6): 1461–1474. https://doi.org/10.1016/j.biocon.2008.04.011
  • Otavo SE, Parrado-Rosselli A, Noriega JA (2013) Superfamilia Scarabaeoidea (Insecta: Coleoptera) como elemento bioindicador de perturbación antropogénica en un parque nacional amazónico. Revista de Biología Tropical 61(2): 735–752. https://doi.org/10.15517/rbt.v61i2.11219
  • Palacios-Ríos M, Rico-Grey V, Fuentes E (1990) Inventario preliminar de los Coleoptera Lamellicornia de la zona de Yaxchilán, Chiapas, México. Folia Entomologica Mexicana 78: 49–60.
  • Peraza L, Deloya C (2006) Una nueva especie mexicana de Dichotomius Hope (Coleoptera: Scarabaeidae) y clave para la identificación de las especies del grupo carolinus. Neotropical Entomology 35(5): 629–631. https://doi.org/10.1590/S1519-566X2006000500009
  • R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
  • Reyes-Novelo E, Delfín-González H, Morón MA (2007) Copro-necrophagous beetle (Coleoptera: Scarabaeidae) diversity in an agroecosystem in Yucatan, Mexico. Revista de Biología Tropical 55(1): 83–99. https://doi.org/10.15517/rbt.v55i1.6059
  • Rivera-Cervantes LE, Halffter G (1999) Monografía de las especies mexicanas de Canthon del subgénero Glaphyrocanthon (Coleoptera: Scarabaeidae: Scarabaeinae). Acta Zoológica Mexicana (n.s. ) 77: 23–150.
  • Roy A, Devi BSS, Debnath B, Murthy MSR (2010) Geospatial modelling for identification of potential ecological corridors in Orissa. Photonirvachak (Dehra Dun) 38(3): 387–399. https://doi.org/10.1007/s12524-010-0042-6
  • Sánchez-de-Jesús HA, Arroyo-Rodríguez V, Andresen E, Escobar F (2016) Forest loss and matrix composition are the major drivers shaping dung beetle assemblages in a fragmented rainforest. Landscape Ecology 31(8): 843–854. https://doi.org/10.1007/s10980-015-0293-2
  • Sánchez-Hernández G, Chamé-Vázquez ER, Gómez B (2019) Nuevos datos de distribución para escarabajos del estiércol (Coleoptera: Scarabaeidae: Scarabaeinae) en México. Revista Chilena de Entomologia 45(4): 415–419. https://doi.org/10.35249/rche.45.4.19.02
  • Sánchez-Hernández G, Gómez B (2018) First precise locality data for Onthophagus atriglabrus Howden & Gill and new state record for Onthophagus anewtoni Howden and Génier (Coleoptera: Scarabaeidae: Scarabaeinae) in Mexico. Coleopterists Bulletin 72(4): 873–877. https://doi.org/10.1649/0010-065X-72.4.873
  • Sánchez-Hernández G, Gómez B, Delgado L, Rodríguez-López EM (2017) Primer registro de Onthophagus longimanus Bates, 1887 (Coleoptera: Scarabaeidae: Scarabaeinae) en Chiapas, México. Dugesiana 24(1): 57–59.
  • Sánchez-Hernández G, Gómez B, Delgado L, Rodríguez-López EM, Chamé-Vázquez ER (2018) Diversidad de escarabajos copronecrófagos (Coleoptera: Scarabaeidae: Scarabaeinae) en la Reserva de la Biosfera Selva El Ocote, Chiapas, México. Caldasia 40(1): 144–160. https://doi.org/10.15446/caldasia.v40n1.68602
  • Santos-Heredia C, Andresen E, Zárate DA, Escobar F (2018) Dung beetle and their ecological functions in three agroforestry systems in the Lacandona rainforest of Mexico. Biodiversity and Conservation 27(3): 2379–2392. https://doi.org/10.1007/s10531-018-1542-x
  • Scholtz CH, Davis ALV, Kryger U (2009) Evolutionary Biology and Conservation of Dung Beetles. Pensoft Publishers, Sofia, 567 pp.
  • Schuster JC (1993) Xylopassaloides (Coleoptera: Passalidae) in Mesoamerica: relations, distribution and new species. The Florida Entomologist 76(1): 114–119. https://doi.org/10.2307/3496019
  • Schuster JC, Cano EB, Cardona C (2000) Un método sencillo para priorizar la conservación de los bosques nubosos de Guatemala, usando Passalidae (Coleoptera) como organismos indicadores. Acta zoológica mexicana (n.s. ) 80: 197–209. http://www.scielo.org.mx/pdf/azm/n80/n80a11.pdf
  • Schuster JC, Cano EB, Reyes-Castillo P (2003) Proculus, giant Latin American passalids (Col., Passalidae): a generic, phylogenetic and biogeographic revision. Acta Zoológica Mexicana (n.s. ) 90: 281–306. http://www.scielo.org.mx/pdf/azm/n90/n90a8.pdf
  • Silva FAB, Louzada J, Vaz-de-Mello FZ (2015) A revision of the Deltochilum subgenus Aganhyboma Kolbe, 1893 (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 3925(4): 451–504. https://doi.org/10.11646/zootaxa.3925.4.1
  • Sokolov IM, Kavanaugh DH (2014) The integripennis species group of Geocharidius Jeannel, 1963 (Carabidae, Bembidiini, Anillina) from Nuclear Central America: A taxonomic review with notes about biogeography and speciation. ZooKeys 443: 61–118. https://doi.org/10.3897/zookeys.443.7880
  • Vaz-de-Mello FZ (2008) Synopsis of the new subtribe Scatimina (Coleoptera: Scarabaeidae: Scarabaeinae: Ateuchini), with descriptions of twelve new genera and review of Genieridium, new genus. Zootaxa 1955(1): 1–75. https://doi.org/10.11646/zootaxa.1955.1.1
  • Vaz-de-Mello FZ, Halffter G, Halffter V (2004) A new species of Pedaridium Harold, from Mexico and Guatemala (Coleoptera: Scarabaeidae: Scarabaeinae: Coprini, Ateuchina). Coleopterists Bulletin 58(2): 247–252. https://doi.org/10.1649/614
  • Zunino M, Halffter G (1988) Análisis taxonómico ecológico y biogeográfico de un grupo americano de Onthophagus. Museo Regionale di Scienze Naturale Torino. Monografia 9: 1–211.
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