SciELO - Scientific Electronic Library Online

 
vol.45 issue2Morphophysiological aspects of the digestive tract in IV stage larvae of Bradysia impatiens (Diptera: Sciaridae)Mites associated with blackberry (Rubus sp. cv. Tupy) in two areas of Michoacan, Mexico author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

Indicators

Related links

  • On index processCited by Google
  • Have no similar articlesSimilars in SciELO
  • On index processSimilars in Google

Share


Revista Colombiana de Entomología

Print version ISSN 0120-0488On-line version ISSN 2665-4385

Rev. Colomb. Entomol. vol.45 no.2 Bogotá July/Dec. 2019  Epub Dec 20, 2019

https://doi.org/10.25100/socolen.v45i2.7963 

Sección Básica

Spatial diversity of dung beetle assemblages (Coleoptera: Scarabaeidae: Scarabaeinae) in five ecoregions from Sucre, Colombian Caribbean coast

Diversidad espacial del ensamblaje de escarabajos coprófagos (Coleoptera: Scarabaeidae: Scarabaeinae) en cinco ecorregiones de Sucre, costa Caribe colombiana

Yina Amell-Caez1 

Indradatta Decastro-Arrazola2 
http://orcid.org/0000-0001-6558-5730

Héctor García3 
http://orcid.org/0000-0002-0893-4727

José D. Monroy-G.4 
http://orcid.org/0000-0003-2832-3699

Jorge Ari Noriega5 
http://orcid.org/0000-0003-1760-7020

1 B. Sc. Biología, Universidad del Magdalena, Santa Marta, Colombia, yinamellbio@gmail.com.

2 Ph. D. Departamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias Naturales, Madrid, España, indra@mncn.csic.es.

3 B. Sc. Universidad del Magdalena, Santa Marta, Colombia, coleopterocoprofago@yahoo.es.

4 M. Sc. Laboratorio de Zoología y Ecología Animal - LAZOEA, Universidad de Los Andes, Bogotá, Colombia, dannielmonroy@gmail.com.

5 Ph. D. Departamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias Naturales, Madrid, España. Laboratorio de Zoología y Ecología Animal - LAZOEA, Universidad de Los Andes, Bogotá, Colombia, jnorieg@hotmail.com.


Abstract

Biodiversity changes in space and time generate complex gradients. These gradients affect community structures, generating beta diversity replacement patterns. The two main patterns of spatial replacement are turnover and nestedness. However, there are very few studies that analyze diversity changes along environmental gradients in the Colombian Caribbean region. In an attempt to understand these spatial changes, a complete sampling was conducted in five Colombian Caribbean ecoregions (Golfo de Morrosquillo, Montes de María, Sabanas, San Jorge, and La Mojana) using dung beetles as an indicator. In each region, a linear transect with 20 pitfall traps baited with dung was established. Differences in abundance, richness, Shannon-index, evenness, and beta diversity between ecoregions were evaluated. A total of 923 individuals belonging to 27 species were collected. The tribe Deltochilini and the genus Canthon were the most diverse. The most abundant species was Silvicanthon aequinoctialis. Significant differences were found in the parameters measured between the ecoregions. A Beta diversity index established a clear spatial pattern demonstrating high turnover with low nestedness values. The Montes de María ecoregion has the highest diversity, which was linked with the maintenance of conserved forest fragments. It is advisable to generate conservation strategies and the designation of a new National Natural Park for Montes de María in order to stop the negative impact caused by agricultural and cattle farming expansion in the region. This study represents the first effort to understand dung beetle spatial patterns within the ecoregions of the Colombian Caribbean region through connecting environmental gradients and spatial diversity dynamics.

Keywords: Bioindicators; beta diversity; ecoregions; Scarabaeidae; spatial heterogenity; Colombia; Neotropical region

Resumen

La biodiversidad cambia en el espacio-tiempo generando gradientes complejos. Estos gradientes afectan la estructura de las comunidades creando dos posibles patrones de recambio espacial, reemplazo o anidamiento. Existen pocos estudios que busquen analizar los cambios de la diversidad a lo largo de gradientes ambientales en la región Caribe de Colombia. Buscando entender estos cambios, se realizó un muestreo en cinco ecorregiones del Caribe colombiano (Golfo de Morrosquillo, Montes de María, Sabanas, San Jorge y La Mojana) usando a los escarabajos coprófagos como un grupo bioindicador. En cada región se estableció un transecto lineal con 20 trampas de caída cebadas con excremento. Se evaluaron las diferencias en la abundancia, riqueza, Shannon-índice, equidad y grupos funcionales entre ecorregiones y condiciones ambientales. Un total de 923 individuos pertenecientes a 27 especies fue recolectado. La tribu Deltochilini y el género Canthon fueron los más diversos. La especie más abundante fue Silvicanthon aequinoctialis. Se encontraron diferencias significativas en los parámetros medidos entre las ecorregiones. La diversidad Beta presenta un claro patrón espacial demostrando un alto recambio y un bajo anidamiento. Los Montes de María presentaron la mayor diversidad, asociada con la conservación de fragmentos de bosque. Es fundamental generar estrategias de conservación y crear un nuevo Parque Nacional Natural para los Montes de María, previniendo el impacto negativo causado por la expansión de la frontera agrícola y ganadera. Finalmente, este estudio representa un primer esfuerzo para entender los patrones espaciales de los escarabajos coprófagos en el Caribe colombiano, relacionando los gradientes ambientales con la dinámica espacial de la diversidad.

Palabras clave: Bioindicadores; diversidad beta; ecorregiones; Scarabaeidae; heterogeneidad espacial; Colombia; región Neotropical

Introduction

Biodiversity changes in space and time, following complex interactions between gradients, such as altitude, precipitation or temperature (Sanders and Rahbek 2012). Some of the best-known gradients in different regions of the world are those associated to changes in space, such as altitude and latitude (Willig et al. 2003). Along these spatial gradient’s biodiversity can present replacement patterns in beta diversity that affect community structure and dynamics (Myers and LaManna 2016). Beta diversity can change in space evidencing two easily recognizable patterns that are antagonistic in nature, namely turnover (i.e., replacement of established species by new ones) and nestedness (i.e., a non-random process of species loss without replacement generating a subset of the biota of richer sites) (Baselga 2010). Despite their importance, there are few studies that analyze spatial patterns of species turnover diversity along environmental gradients in the Neotropical region (Escobar 1997; Barraza et al. 2010; Louzada et al. 2010; Silva and Hernández 2016; Villada-Bedoya et al. 2017).

One of the most interesting biogeographical regions in the Neotropics for analyzing spatial turnover is the Caribbean region of Colombia. This area consists of seven Departments (i.e., Atlántico, Bolívar, Cesar, Córdoba, La Guajira, Magdalena, and Sucre) encompassing a broad variety of ecosystems (i.e., dry and rainy forests, mountain forests, valleys, savannas, swamps, and mangroves) with a strong environmental gradient reaching from the dry coastal areas to the extremely humid areas in the interior (Rangel-Ch. and Carvajal-Cogollo 2012; IDEAM 2013). Within the Caribbean region, the Sucre department is one of the Colombian areas with the greatest spatial heterogeneity, presenting a marked environmental gradient that ranges from its coastal dry forests to the extreme humidity of its flooded marshes and the San Jorge and Cauca river basin systems (Aguilera 2005). This diversity in landscape, climate, topography, and vegetation is reflected in the five subregions of the department. Despite the great diversity that defines this area, the ecosystems of the Colombian Caribbean have been severely affected in the last decades by human intervention due to livestock breeding, agriculture, and mining (Rudas et al. 2007); a situation that has brought up the necessity to search for strategies that can evaluate the degree of disturbance caused by these activities within them.

A recurrent strategy applied to evaluate anthropological perturbation on biodiversity is the use of bioindicators that allow the estimation and quantification of the degree of environmental disturbance. For this purpose, the dung beetles of the subfamily Scarabaeinae (Coleoptera: Scarabaeidae) are frequently employed, having been used in different regions of the world as an effective bioindicator group to evaluate and monitor the status of ecosystem health and its conservation (Halffter and Favila 1993; McGeoch et al. 2002; Spector 2006; Nichols et al. 2007; Otavo et al. 2013). The intimate association between this group and vertebrate excrement has important consequences in ecosystem function, contributing to nutrient cycling, soil aeriation, parasite control, and seed dispersal (Nichols et al. 2008).

The Sucre Caribbean region in Colombia presents one of the largest knowledge gaps in dung beetles biodiversity patterns in the country due to the lack of appropriate studies (Noriega et al. 2013; 2015). Therefore, the main objective of the current study is to analyze the spatial turnover and its effects on the biodiversity of dung beetle’s assemblages within the five ecoregions of the Sucre department in the Colombian Caribbean region. The main questions were: How biodiversity changes between the different ecoregions of the Sucre department?, and whether or not these changes present a relationship with spatial environmental variations in temperature, precipitation, and/or humidity? It was hypothesized that the change in dung beetle composition along the assemblages in Sucre will be due to spatial turnover rather than species loss (nestedness), and that the biodiversity maximum will coincide with the optimal environmental conditions for this bioindicator group.

Materials and methods

Study area

The Sucre Department, in the Caribbean region at the north of Colombia (between 10º08’03” - 08º16’46”N and 74º32’35” - 75º42’25”W) has an extension of 10,364 km2 (Peroza and De la Ossa 1997). The climate is warm with an aridity gradient stretching from dry coastal areas to the more humid areas around the San Jorge river basin. Average annual temperatures oscillate between 25.5 and 28.7° C, average humidity is 85 % and seasonality is bimodal with two rainy seasons that alternate with dry ones. Rainfall values vary greatly from 1,000 mm along the coastal strip to 3,000 mm in the lower San Jorge region (Aguilera 2005). These environmental gradients originate five physiographic ecoregions within the Sucre department: 1) Golfo de Morrosquillo, 2) Montes de María, 3) Sabanas, 4) San Jorge, and 5) La Mojana (Fig. 1).

Figure 1 Location and climatic characteristics of the studied areas: A. Map of the ecoregions in the Sucre Department and sampling sites: (1) Morrosquillo (Mpio. Coveñas), (2) Montes de María (Mpio. Coloso), (3) Sabanas (Mpio. Buenavista), (4) San Jorge (Mpio. La Union), and (5) Mojana (Mpio. Sucre). B. Ecoregional annual precipitation map. C. Ecoregional variation in annual precipitation and temperature. D. Geographical coordinates of sampled locations and environmental values (T: average annual temperature, P: average annual precipitation, and H: average annual relative humidity). 

Dung beetle sampling

Sample collections were carried out during the rainy season between September and October 2011. One observation station was chosen in each of the five ecoregions (Fig. 1, Table 1), taking into consideration the access routes, conservation status, and the biogeographical and ecological characteristics of each ecoregion. Pitfall traps consisting in 500 ml plastic cups with a diameter of 10 cm and containing 300 ml of 70 % ethanol were buried at ground level (Noriega and Fagua 2009). The bait (50 g mixed 1:1 human-pig excrement) was wrapped in gauze and suspended with a wire above the trap. A white plastic plate was suspended above the trap with another wire, preventing the bait from desiccation and from rainfall. Traps were placed along two 500 m linear transects separated 100 m from each other. Each transect consisted of 10 traps separated 50 m from each other (Larsen and Forsyth 2005), consisting of a total of 20 traps per station and 100 traps for the five ecoregions. Traps were baited at 17 h and maintained for 72 h.

Sample processing

Samples were preserved in 70 % ethanol and their number, transect, and ecoregion recorded. Specimens were then deposited at the Entomological Laboratory of the Universidad del Magdalena (INTROPIC) where morph types were generated. Species identification was carried out at the Zoology and Aquatic Ecology Laboratory of the Universidad de Los Andes (LAZOEA) based on taxonomical keys (Edmonds 1994; Kohlmann and Solis 2001; Solis and Kohlmann 2002; Camero 2010; Vaz-de-Mello et al. 2011). Each species was allocated to a trophic relocation guild (i.e., paracoprids, telecoprids, and endocoprids) following the traditional classification (Halffter and Edmonds 1982; Doube 1990) and the dung-relocation behavior of each genus. Individuals were mounted, labelled, and deposited at the Universidad del Magdalena Entomological Collection (CEUM) and the last author reference collection (CJAN).

Environmental values

Three bioclimatic variables: annual average temperature (°C), annual average precipitation (mm), and annual average humidity (%) of WorldClim were used (see www.worldclim.org; Hijmans et al. 2005), at a resolution of 2.5 minutes (approximately 25 km2), as environmental predictors (Fig. 1).

Tabla 1 Diversity of dung beetles present within the five ecoregions. (1) Morrosquillo, (2) Montes de María, (3) Sabanas, (4) San Jorge, and (5) Mojana of the Sucre Department, Colombian Caribbean. Relocation guilds (G): paracoprids (P), telecoprids (T), and endocoprids (E). 

Tribe Species G Ecoregions Total (%)
1 2 3 4 5
Ateuchini Ateuchus sp. 1 P 0 3 0 0 0 3 (0.3)
Ateuchus sp. 2 P 0 4 0 0 0 4 (0.4)
Coprini Canthidium euchalceum Balthasar, 1939 P 0 4 0 0 0 4 (0.4)
Canthidium aurifex Bates, 1887 P 0 5 0 0 0 5 (0.5)
Dichotomius cf. agenor (Harold, 1869) P 4 30 0 0 0 34 (3.7)
Coptodactylini Uroxys sp. 1 P 0 3 0 0 0 3 (0.3)
Uroxys sp. 2 P 0 1 0 0 0 1 (0.1)
Uroxys sp. 3 P 0 5 0 0 0 5 (0.5)
Uroxys sp. 4 P 0 9 0 0 0 9 (1.0)
Deltochilini Sylvicanthon aequinoctialis (Harold, 1868) T 0 370 0 0 0 370 (40.1)
Canthon cyanellus Harold, 1863 T 0 2 0 0 0 2 (0.2)
Canthon juvencus (Harold, 1868) T 0 0 0 4 3 7 (0.8)
Canthon mutabilis Lucas, 1857 T 0 0 14 0 0 14 (1.5)
Canthon lituratus (Germar, 1813) T 3 5 2 0 0 10 (1.1)
Canthon septemmaculatus (Latreille, 1811) T 3 7 0 0 0 10 (1.1)
Canthon subhyalinus Harold, 1867 T 0 18 0 0 0 18 (2.0)
Deltochilum guildingii (Westwood, 1835) T 0 10 0 0 0 10 (1.1)
Pseudocanthon perplexus (LeConte, 1847) T 13 0 0 4 82 99 (10.7)
Demarziellini Trichillidium pilosum (Robinson, 1948) P 0 5 0 0 0 5 (0.5)
Oniticellini Eurysternus caribaeus (Herbst, 1789) E 2 7 0 0 0 9 (1.0)
Onthophagini Digitonthophagus gazella (Fabricius, 1787) P 12 0 0 0 0 12 (1.3)
Onthophagus acuminatus Harold, 1880 P 0 9 0 0 0 9 (1.0)
Onthophagus marginicollis Harold, 1880 P 15 63 12 70 6 166 (18.0)
Onthophagus landolti P 0 61 0 24 0 85 (9.2)
Onthophagus cf. clypeatus Blanchard, 1843 P 0 16 0 0 0 16 (1.7)
Onthophagus sp. 1 P 0 1 0 3 0 4 (0.4)
Phanaeini Phanaeus hermes Harold, 1868 P 0 9 0 0 0 9 (1.0)
Abundance 52 647 28 105 91 923
Richness 7 23 3 5 3 27
Margalef index (d) 1.87 3.55 0.98 1.14 0.57 -
Shannon index (H') 1.66 1.72 0.85 0.94 0.47 -
Pielou index (J') 0.85 0.56 0.62 0.58 0.43 -

Data analysis

Relative species abundances were evaluated by means of species accumulation curves in EstimateS v. 8.2 (Colwell 2011). Alfa diversity was described using the total number of species (S), Margalef’s richness parameter (d), the Shannon-Wiener index (H’), and Pielou’s evenness index (J’) with PRIMER 6.0 (Clarke and Gorley 2006). Normality in the data was checked with the Shapiro-Wilk test and homogeneity of variances with Bartlett’s test. To determine whether there were differences between abundance and richness between ecoregions a Kruskall-Wallis test was performed in Statistix v. 8.1 with a significance threshold of α = 0.05. The similarity between ecoregions was estimated with the Jaccard (Ij) and Sorensen indexes (Is) (Moreno 2001). Beta diversity was assessed with the index proposed by Baselga (2010) , which decomposes total beta diversity into turnover and nestedness components (βSIM: Simpson dissimilarity - spatial turnover, βNES: nestedness dissimilarity, and βSOR: Sørensen dissimilarity - total Beta diversity; measuring additive fractions: βSOR = βSIM + βNES) performed in R v. 3.1.1 program (R Development Core Team 2016), using the betapart package (Baselga and Orme 2012). Likewise, the Colwell and Coddington (1994) complementarity index was calculated to understand the composition overlap of assemblages. An NMDS (non-metric multidimensional scaling) analysis of the Bray-Curtis similarity index, transforming the abundances to log (x + 1) (Clarke and Gorley 2006), was performed in PRIMER v. 6 (Clarke and Gorley 2006) to determine spatial turnover between ecoregions considering abundance of species.

Results

Interpretation of the sampling effort curves for each ecoregion evidence that the number of observed species was above 90 % of the total species expected (1 = 95 - 100 %, 2 = 90 - 100 %, 3 = 99-100 %, 4 = 97 - 100 %, 5 = 99 - 100 %) when applying the values for singletons, doubletons, and the ACE, Chao 1, Chao 2, and Jack 1 indexes (Fig. 2). These values demonstrate that the number of traps used was adequate to sample a representative percentage of species of the dung beetle assemblage within the five ecoregions.

Figure 2 Sampling effort curves for the dung beetle’s species (Coleoptera: Scarabaeinae) in the five ecoregions: (1) Morrosquillo, (2) Montes de María, (3) Sabanas, (4) San Jorge, and (5) Mojana, Sucre Department, Colombian Caribbean. N = 20 traps per region. 

Composition, abundance, richness, and functional guilds

A total of 923 individuals were collected belonging to 27 species, 12 genera, and eight tribes (Table 1). The tribe with the largest number of species was Deltochilini (n = 9), followed by Onthophagini (n = 6). Canthon was the most diverse genera with six species (Table 1). The species Pseudocanthon perplexus (LeConte, 1847) was registered for the first time within the Sucre department. The most abundant species was Sylvicanthon aequinoctialis (Harold, 1868) (n = 370, 40.08 %), followed by O. marginicollis Harold, 1880 (n = 166, 17 %), and P. perplexus (n = 99, 10 %) (Table 1). Significant differences in abundance (H = 49.61, P ≤ 0.001, n = 20; Fig. 3A ) and richness (H = 50.75, P ≤ 0.001, n = 20; Fig. 3B ) were observed between ecoregion stations. Twenty-three species (n = 647) were collected at station 2, seven (n = 52) at station 1, five (n = 105) at station 4, four (n = 28) at station 3, and three (n = 91) at station 5 (Table 1, Fig. 3). Ecoregion 2 registered the highest Margalef’s richness index (d = 3.55) and the highest Shannon-Wiener value (H’ = 1.72), while ecoregion 5 the smallest value (Table 1). Evenness values (J’) displayed large differences between ecoregions, from 0.85 (ecoregion 1) to 0.43 (ecoregion 5) (Table 1). In relation to the functional guilds, 17 species were paracoprids (tunnelers, 63.0 %), nine telecoprids (rollers, 67.8 %), and one endocoprid (dweller, 3.7 %) (Table 1, Fig. 4). Species from ecoregions 2 and 4 tended to be paracoprids (67.8 %, n = 19), while those from ecoregions 3 and 5 were predominantly telecoprids (66.6 %, n = 4) (Fig. 4). The most abundant guild in ecoregions 2, 3, and 5 was the telecoprids (66.9 %, n = 513), while in 1 and 4 paracoprids were most abundant (81.5 %, n = 128) (Fig. 4).

Figure 3 Boxplots illustrating differences in: A. Abundance and B. Richness between the five ecoregions of the Sucre Department, Colombia. N = 20 traps per region. 

Figure 4 Cumulative percentage of: A. Number of species and B. Number of individuals classified by relocation guild (paracoprids, telecoprids, and endocoprids) in the five ecoregions: (1) Morrosquillo, (2) Montes de María, (3) Sabanas, (4) San Jorge, and (5) Mojana, of the Sucre Department, Colombian Caribbean. N = 20 traps per region. 

Complementarity, beta diversity, and spatial pattern between regions

The complementarity index (C) revealed that ecoregion 2 was the most dissimilar in relation to species composition, sharing only one species with ecoregion 5 (C = 0.96), but showing similar values with ecoregions 2 and 3 and 2 and 4 (C = 0.92; Table 2); ecoregions 4 and 5 were the most similar with a complementarity index of C = 0.4. The partition of beta diversity index presented an overall high total Beta diversity (βsor > 0.6 in all 5 ecoregions) with a marked pattern of high turnover (βsim around 60-70 % of total Beta) with low nestedness values in the five ecoregions (Bnes around 25 % of total Beta) (Fig. 5). The Sabanas region presented the highest species turnover, and Montes de María the most nested composition (βnes). This pattern is even clearer if abundance is considered, using Bray-Curtis. In addition, the NMDS analysis displayed a spatial separation of the five ecoregions, indicating a strong spatial pattern (Fig. 6).

Table 2 Complementarity analysis between the five ecoregions of the Sucre Department, Colombian Caribbean. In parenthesis: the number of species shared between ecoregions. 

Ecoregions
1 2 3 4 5
Morrosquillo Montes de María Sabanas San Jorge Mojana
1 Morrosquillo - (5) (2) (2) (2)
2 Montes de María 0.81 - (2) (2) (1)
3 Sabanas 0.72 0.92 - (1) (1)
4 San Jorge 0.81 0.92 0.87 - (3)
5 Mojana 0.75 0.96 0.83 0.41 -

Figure 5 Turnover values for: A. Beta (nestedness and turnover) and B. Bray-Curtis (gradient and balanced) indices for the five ecoregions of the Sucre Department, Colombia. N = 20 traps per region. 

Figure 6 NMDS analysis employing the Bray-Curtis similarity index for the dung beetle’s assemblage in the five ecoregions of the Sucre Department, Colombia. 

Environmental values and diversity

The Spearman correlation coefficients for species richness and abundance of dung beetles in the five ecoregions demonstrated that temperature have the highest relationship with richness (r = 0.679) and abundance (r = 0.564), followed by precipitation and humidity (Table 3).

Table 3 Spearman correlation coefficients for species richness and abundance of dung beetles in the five ecoregions versus temperature, precipitation, and humidity in the Sucre Department, Colombian Caribbean. 

Temperature Precipitation Humidity
Richness 0.679 0.522 0.471
Abundance 0.564 0.345 0.261

Discussion

Biodiversity changes in space results in complex interaction gradients that affects the structure of communities (Sanders and Rahbek 2012). One of the most interesting biogeographical regions in the Neotropics for analyzing spatial diversity changes is the Caribbean region of Colombia, due to the high spatial turnover between different ecosystems in a reduce space. Because of this, we asked the following question: How biodiversity changes between different ecoregions of the Sucre department? Using dung beetles as a bioindicator tool we hypothesize that the change in dung beetle diversity between regions will be due to a spatial turnover pattern. In general terms, important differences were observed in abundance, richness, Shannon index, evenness, and functional groups between the different ecoregions. The beta diversity index established a marked spatial pattern demonstrating high turnover and validating our hypothesis. In addition, the results we obtained on this study constitute one of the first efforts to systematically understand dung beetle spatial patterns within the ecoregions of the Colombian Caribbean, including the effects of environmental gradients on the spatial dynamics of diversity.

Composition, abundance, and richness

Species composition, abundance, and richness appear to be in accordance to what has been observed in other studies related to climate seasonality (Janzen 1983; Davis 1996; Andresen 2005; Labidi et al. 2012; Noriega et al. 2016). However, species richness varies substantially between ecoregions, presenting its highest value in the Montes de María region due to an inferior level of perturbation and higher degree of conservation. In addition, this region accommodates the most adequate climatic conditions in temperature, precipitation, and humidity (i.e., 26.8 °C, 1,100 mm, and 75 % humidity; variables strongly related with the conservation level of the vegetation cover) to maintain dung beetles’ populations, as registered in other studies for other regions (Nunes et al. 2016; Silva et al. 2016; Gómez-Cifuentes et al. 2017). Likewise, the low richness observed in other ecoregions may be due to a higher level of perturbation and habitat degradation as a result of extensive livestock breeding (Aguilera 2005). Other possible factors that could contribute to this pattern are the reduction of wild mammal populations, the fragmentation of forests, and especially the growth of agricultural frontier (Gill 1991; Halffter 1991; Escobar 1997). In accordance with the indexes of diversity, a marked difference between ecoregions is observed, that may be related to the typology of the soil that is less compact and humid in forests in contrast to those found in the savannas, which obstruct the establishment of dung beetles since they are lacking a plant cover (Howden and Nealis 1975; Halffter et al. 1992; Estrada and Coates-Estrada 2002).

Of the 12 genera and 27 species registered in this study, P. perplexus is a new record for the Sucre department; this observation evidences the necessity for more in-depth surveys in this area. The species richness encountered in the five ecoregions coincides with those registered in punctual studies within the department (Navarro et al. 2011a, 2011b; Tovar et al. 2016) and with others carried out in the Colombian Caribbean (Noriega et al. 2007; Martínez et al. 2009; Solis et al. 2011; Cárdenas-Bautista et al. 2012; Delgado-Gómez et al. 2012). In this manner, the genus Canthon was the most abundant in all ecoregions as reported by other authors (Jiménez-Ferbans et al. 2008; Martínez et al. 2009, 2010; Solis et al. 2011), suggesting that this taxon is one of the widely distributed in the Colombian Caribbean region. The dominance of tunnelers species in certain ecoregions may be related to the differential availability of trophic resources and with the type of soil; the latter represents a fundamental factor that determines the abundance of this group (Halffter 1991; Hanski and Cambefort 1991; Osberg et al. 1994). The marked abundance of S. aequinoctialis may be attributed to its unambiguous association with primate excrement, which is especially abundant in the Montes de María ecoregion (Galván 2010). Lastly, the presence in the ecoregion of Morrosquillo of an introduced species from Africa (D. gazella (Fabricius, 1787)) that is strongly associated to disturbed areas with livestock (Navarro et al. 2009; Noriega et al. 2011) suggest the high level of perturbation that exists in this area due to an increase in the cattle industry.

Functional guilds and spatial diversity patterns

It was evident that the structure of the assemblage, in terms of the abundance and richness of each ecoregion, affects the presence of the three main functional guilds. The paracoprids were dominant in terms of richness (N = 17 spp.), meanwhile the telecoprids were dominant in abundance (due to the high numbers of S. aequinoctialis, N = 370 ind.). The non-appearance of any endocoprid species in region 3, 4, and 5 corroborate the impoverishment of the assemblage structure in these areas. There is a slight tendency to equilibrium in the proportion between paracoprids and telecoprids in all regions, except on region 2 where the high diversity numbers increase the number of paracoprids species. This high richness (especially of telecoprids) might be also connected to the food resource offer in the area, and especially the presence of primates that could support a high diversity of rollers (Estrada et al. 1993, 1999; Noriega 2012). Furthermore, there is a high proportion of telecoprids species in the Caribbean region in comparison with other areas in Colombia, where the proportion of rollers is lower (Neita and Escobar 2012; Otavo et al. 2013; Villada-Bedoya et al. 2017).

Species turnover was exceptionally different between ecoregions, displaying near zero values for the Jaccard and Sorensen indexes, and demonstrating a marked spatial pattern and strong turnover due to varying environmental conditions. In addition, the complementarity index displayed high values, which indicates that the number of species shared between ecoregions is low. In general terms, there is a strong spatial turnover in species richness (i.e., turnover, Bsim) between the five ecoregions, which increases towards the central area of the environmental gradient (Sabanas ecoregion). Although some species loss (i.e., nestedness, Bnes) is observed in all ecoregions, these values are very low in comparison to the real turnover between them. This pattern is consistent with that observed in studies carried out in other parts of the world presenting accentuated environmental variance (Labidi et al. 2012).

Conservation interest

It is manifest that the Montes de María ecoregion is an area of great biotic importance (Rudas et al. 2007; Rangel-Ch. and Carvajal-Cogollo 2012) regarding it hosts a high richness of dung beetle species associated to the remaining forest fragments in this region. Our results suggest that the five ecoregions are strikingly different in their species assemblage structure since they presented few similarities in their composition, abundance, and richness. The diversity of the dung beetle’s assemblage exhibits a spatial pattern associated to the heterogeneity of the landscape, conservation status of the forest cover, climate, and soil use in this region (Aguilera 2005). A decline in the diversity associated with environmental variation, conservation status, change of ecosystem function, and degree of soil compaction was observed.

It is essential to propose and generate conservation strategies for the Montes de María ecoregion in the interest of potentially creating a novel conservation zone and the designation of a new National Natural Park. At present, the Sucre department only counts with two protected area systems, which shares with the Bolivar Department: (1) PNN Islas del Rosario and San Bernardo in ocean territory, and (2) Santuario de Fauna y Flora El Corchal El Mono Hernández in the continental territory. This sanctuary was created in 2002 for protection of the mangroves and has a surface area of 38.5 km2, of which little more than 50 % is located within the Sucre Department. This makes Sucre at the national level one of the departments with the lowest percentage of protected areas in Colombia (less than 0.02 % of 142,682 km2 in total) (SINAP 2018). Furthermore, the existing reserves in the region should be enlarged to increase the spatial connection between small and medium forest fragments with existing corridors. Finally, it is important to generate governmental strategies at the municipal and departmental levels to try to stop the negative impact caused by the expansion of the agricultural and cattle farming into the Caribbean region.

The degree of fragmentation and the loss of vegetation cover to which the few remaining forest relicts are subjected in this region generate a marked effect in the registered biodiversity. The extension of the agricultural and cattle farming frontier has caused a sharp decline in the diversity of this group of insects; bioindicators that have been evidenced to play an irreplaceable role in the stability and functionality of the ecosystems where they inhabit. It is crucial to continue performing similar studies in this area on a landscape scale with the purpose of contributing to the understanding of how the different agricultural and livestock practices influence ecosystem degradation in the ecoregions, and consequently develop management and conservation strategies.

Acknowledgements

To Emilio Realpe and the Zoology and Aquatic Ecology Laboratory - LAZOEA, of the Universidad de Los Andes. To Javier Santos and David Morris for checking the English version of this article. To Darren Mann for his priceless help in the identification and confirmation of several of the species sampled. To the Biology program at the Faculty of Ciencias Básicas of the Universidad del Magdalena. We thank the provincial community and local authorities that helped in each of the municipalities where the fieldwork was carried out. We are grateful to the comments and suggestions of two anonymous reviewers and the editor in chief of the journal that improved the quality of the paper.

Literature cited

AGUILERA, M. M. 2005. La economía del departamento de Sucre: Ganadería y sector público. Documentos de Trabajo sobre Economía Regional. Banco de la República. Centro de Estudios Económicos Regionales (CEER), Cartagena de Indias, Colombia. 126 p. [ Links ]

ANDRESEN, E. 2005. Effects of season and vegetation type on community organization of dung beetles in a tropical dry forest. Biotropica 37: 291-300. https://doi.org/10.1111/j.1744-7429.2005.00039.xLinks ]

BARRAZA, J.; MONTES, J.; MARTÍNEZ, N.; DELOYA, C. 2010. Ensamblaje de escarabajos coprófagos (Scarabaeidae: Scarabaeinae) del bosque tropical seco, Bahía Concha, Santa Marta (Colombia). Revista Colombiana de Entomología 36 (2): 285-291. [ Links ]

BASELGA, A. 2010. Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography 19: 134-143. https://doi.org/10.1111/j.1466-8238.2009.00490.xLinks ]

BASELGA, A.; ORME, C. D. L. 2012. Betapart: an R package for the study of beta diversity. Methods in Ecology and Evolution 3: 808-812. https://doi.org/10.1111/j.2041-210X.2012.00224.xLinks ]

CAMERO, E. 2010. Los escarabajos del género Eurysternus Dalman, 1824 (Coleoptera: Scarabaeidae) de Colombia. Boletín de la Sociedad Entomológica Aragonesa 46: 147-179. [ Links ]

CÁRDENAS-BAUTISTA, J.; MORALES-CASTAÑO, I. T.; CARVAJAL-COGOLLO, J. E. 2012. Escarabajos coprófagos (Scarabaeidae: Scarabaeinae) en dos fragmentos de bosque y su matriz circundante en el Caribe Colombiano. pp. 821-831. En: Rangel-Ch., J. O. (Ed.). Colombia Diversidad Biótica XII: La región Caribe de Colombia. Instituto de Ciencias Naturales, Bogotá. 1046 p. [ Links ]

CLARKE, K. R.; GORLEY, R. N. 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth. [ Links ]

COLWELL, R. K. 2011. EstimateS, Version 8.2: Statistical Estimation of Species Richness and Shared Species from Samples (Software and User’s Guide). [ Links ]

COLWELL, R.; CODDINGTON, J. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 345: 101-118. https://doi.org/10.1098/rstb.1994.0091Links ]

DAVIS, A. 1996. Seasonal dung beetle activity and dung dispersal in selected South African habitats: Implications for pasture improvement in Australia. Agriculture, Ecosystems and Environment 58: 157-169. https://doi.org/10.1016/0167-8809(96)01030-4Links ]

DELGADO-GÓMEZ, P.; LOPERA, A.; RANGEL-CH., J. O. 2012. Variación espacial del ensamblaje de escarabajos coprófagos (Scarabaeidae: Scarabaeinae) en remanentes de bosque seco en Chimichagua (Cesar, Colombia). pp. 833-849. En: Rangel-Ch., J. O. (Ed.). Colombia Diversidad Biótica XII: La región Caribe de Colombia. Instituto de Ciencias Naturales, Bogotá. 1046 p. [ Links ]

DOUBE, B. 1990. A functional classification for analysis of the structure of dung beetle assemblages. Ecological Entomology 15: 371-383. https://doi.org/10.1111/j.1365-2311.1990.tb00820.xLinks ]

EDMONDS, W. D. 1994. Revision of Phanaeus Macleay, a new world genus of Scarabaeine dung beetles (Coleoptera, Scarabaedae, Scarabaeinae). Natural History Museum of the Angeles Country. Contributions in Science 443: 1-105. [ Links ]

ESCOBAR, F. 1997. Estudio de la comunidad de coleópteros coprófagos (Scarabaeidae) en un remanente de bosque seco al norte del Tolima Colombia. Caldasia 19 (3): 419-430. [ Links ]

ESTRADA, A.; COATES-ESTRADA, R. 2002. Dung beetles in continuous forest, forest fragments and in an agricultural mosaic habitat island at los Tuxtlas, Mexico. Biodiversity and Conservation 11: 1093-1918. https://doi.org/10.1016/S0006-3207(01)00135-5Links ]

ESTRADA, A.; HALFFTER, G.; COATES-ESTRADA, R.; MERRIT, D. A. 1993. Dung beetles attracted to mammalian hervibore (Alouatta palliata) and omnivore (Nasua narica) dung in the tropical rain forest of Los Tuxtlas, Mexico. Journal of Tropical Ecology 9 (1): 45-54. https://doi.org/10.1017/S0266467400006933Links ]

ESTRADA, A.; ANZURES, A.; COATES-ESTRADA, R. 1999. Tropical rain forest fragmentation, Howler monkeys (Alouatta palliata), and dung beetles at Los Tuxtlas, Mexico. American Journal of Primatology 48: 253-262. https://doi.org/10.1002/(SICI)1098-2345(1999)48:4<253::AID-AJP1>3.0.CO;2-DLinks ]

GALVÁN, S. 2010. Mamíferos y aves silvestres registrados en una zona de los Montes de María, Colosó, Sucre, Colombia. Revista Colombiana de Ciencia Animal 2 (1): 45-57. https://doi.org/10.24188/recia.v2.n1.2010.327Links ]

GILL, B. 1991. Dung beetles in tropical American forests. pp. 211-229. En: Hanski I.; Cambefort, Y. (Eds.). Dung beetle ecology. Princeton University Press. New Jersey. 481 p. https://doi.org/10.1515/9781400862092.211Links ]

GÓMEZ-CIFUENTES, A.; MUNEVAR, A.; GIMÉNEZ, V. C.; GATTI, M. G.; ZURITA, G. A. 2017. Influence of land use on the taxonomic and functional diversity of dung beetles (Coleoptera: Scarabaeinae) in the southern Atlantic forest of Argentina. Journal of Insect Conservation 21 (1): 147-156. https://doi.org/10.1007/s10841-017-9964-4Links ]

HALFFTER, G. 1991. Historical and ecological factors determining geographical distribution of beetles (Coleoptera: Scarabaeidae: Scarabaeinae). Folia Entomológica Mexicana 82: 195-238. https://doi.org/10.21426/B615110376Links ]

HALFFTER, G.; EDMONDS, D. 1982. The nesting behaviour of dung beetles. An ecological and evolutive approach. Instituto de Ecología. México D. F. 176 p. [ Links ]

HALFFTER, G.; FAVILA, M. E. 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. [ Links ]

HALFFTER, G.; FAVILA, M. F.; HALFFTER, V. 1992. A comparative study of the structure of the scarab guild in Mexican Tropical Rain Forest and derived ecosystem. Folia Entomológica Mexicana 84: 131-156. [ Links ]

HANSKI, I.; CAMBEFORT, Y. 1991. Dung beetle ecology. Princeton University Press, Princeton, New Jersey. Insecta Mundi 0129: 1-111. https://doi.org/10.1515/9781400862092Links ]

HIJMANS, R. J.; CAMERON, S. E.; PARRA, J. L.; JONES, P. G.; JARVIS, A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25 (15): 1965-1978. https://doi.org/10.1002/joc.1276Links ]

HOWDEN, H.; NEALIS, V. 1975. Effects of clearing in a tropical rain forest on the composition of the coprophagous scarab beetle fauna (Coleoptera). Biotropica 7 (2): 77-83. https://doi.org/10.2307/2989750Links ]

IDEAM. 2013. Zonificación y codificación de unidades hidrográficas e hidrogeológicas de Colombia. 2013. Instituto de Hidrología, Meteorología y Estudios Ambientales, Bogotá, D. C., Colombia. 46 p. [ Links ]

JANZEN, D. H. 1983. Seasonal change in abundance of large nocturnal dung beetles (Scarabaeidae) in a Costa Rican deciduous forest and adjacent horse pasture. Oikos 41: 274-283. https://doi.org/10.2307/3544274Links ]

JIMÉNEZ-FERBANS, L.; MENDIETA-OTÁLORA, W.; GARCÍA, H.; AMAT-GARCÍA, G. 2008. Notas sobre los escarabajos coprófagos (Coleoptera: Scarabaeinae) en ambientes secos de la región de Santa Marta, Colombia. Acta Biológica Colombiana 13 (2): 203-208. [ Links ]

KOHLMANN, B.; SOLIS, A. 2001. El género Onthophagus (Coleoptera: Scarabaeidae) en Costa Rica. Giornale Italiano di Entomologia 49 (9): 159-261. [ Links ]

LABIDI, I.; ERROUISSI, F.; NOUIRA, S. 2012. Spatial and temporal variation in species composition, diversity, and structure of Mediterranean dung beetle assemblages (Coleoptera: Scarabaeidae) across a bioclimatic gradient. Environmental Entomology 41 (4): 785-801. https://doi.org/10.1603/EN11278Links ]

LARSEN, T.; FORSYTH, A. 2005. Trap spacing and transect design for dung beetle biodiversity studies. Biotropica 37 (2): 322-325. https://doi.org/10.1111/j.1744-7429.2005.00042.xLinks ]

LOUZADA, J.; LIMA, A. P.; MATAVELLI, R.; ZAMBALDI, L.; BARLOW, J. 2010. Community structure of dung beetles in Amazonian savannas: role of fire disturbance, vegetation and landscape structure. Landscape Ecology 25 (4): 631-641. https://doi.org/10.1007/s10980-010-9448-3Links ]

MARTÍNEZ, N.; GARCÍA, H.; PULIDO, L.; OSPINO, D.; NARVÁEZ, J. 2009. Escarabajos coprófagos (Coleoptera: Scarabaeinae) de la vertiente noroccidental, Sierra Nevada de Santa Marta, Colombia. Neotropical Entomology 38 (6): 708-715. https://doi.org/10.1590/S1519-566X2009000600002Links ]

MARTÍNEZ, N.; CAÑAS, L.; RANGEL, J.; BARRAZA, J.; MONTES, J.; BLANCO, O. 2010. Coleópteros coprófagos (Scarabaeidae: Scarabaeinae) en un fragmento de bosque seco tropical en el departamento del Atlántico, Colombia. Boletín del Museo de Entomología de la Universidad del Valle 11 (1): 21-30. [ Links ]

MCGEOCH, M.; VAN RENSBURG, B.; BOTES, A. 2002. The verification and application of bioindicators: a case study of dung beetles in savanna ecosystem. The Journal of Applied Ecology 39 (4): 661-672. https://doi.org/10.1046/j.1365-2664.2002.00743.xLinks ]

MORENO, C. E. 2001. Métodos para medir la biodiversidad. M&T-Manuales y Tesis SEA, Zaragoza, 84 p. [ Links ]

MYERS, J. A.; LAMANNA, J. A. 2016. The promise and pitfalls of β-diversity in ecology and conservation. Journal of Vegetation Science 27: 1081-1083. https://doi.org/10.1111/jvs.12482Links ]

NAVARRO, I. L.; ROMAN, A. K.; GÓMEZ, F. H.; PÉREZ, H. A. 2009. Primer registro de Digitonthophagus gazella (Fabricius, 1787) para el Departamento de Sucre, Colombia. Revista Colombiana de Ciencia Animal 1 (1): 60-64. https://doi.org/10.24188/recia.v1.n1.2009.410Links ]

NAVARRO, I. L.; ROMAN, A. K.; GÓMEZ, F. H.; PÉREZ, H. A. 2011a. Variación estacional en escarabajos coprófagos (Coleoptera: Scarabaeidae: Scarabaeinae) de la Serranía de Coraza, Sucre (Colombia). Revista Colombiana de Ciencia Animal 3 (1): 102-110. https://doi.org/10.24188/recia.v3.n1.2011.330Links ]

NAVARRO, I. L.; ROMAN, A. K.; GÓMEZ, F. H.; PÉREZ, H. A. 2011b. Listado de escarabajos coprófagos (Coleoptera: Scarabaeidae: Scarabaeinae) de la Serranía de Coraza, Sucre (Colombia). Revista Colombiana de Ciencia Animal 3 (2): 262-268. https://doi.org/10.24188/recia.v3.n2.2011.375Links ]

NEITA, J. C.; ESCOBAR, F. 2012. The potential value of agroforestry to dung beetle diversity in the wet tropical forests of the Pacific lowlands of Colombia. Agroforest Systems 85 (1): 121-131. https://doi.org/10.1007/s10457-011-9445-9Links ]

NICHOLS, E.; LARSEN, T.; SPECTOR, S.; DAVIS, A. L.; ESCOBAR, F.; FAVILA, M.; VULINEC, 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.2007.01.023Links ]

NICHOLS, E.; SPECTOR, S.; LOUZADA, J.; LARSEN, T.; AMEZQUITA, S.; FAVILA, M.; NETWORK, T. S. R. 2008. Ecological functions and ecosystem services of Scarabaeinae dung beetles. Biological Conservation 141 (6): 1461-1474. https://doi.org/10.1016/j.biocon.2008.04.011Links ]

NORIEGA, J. A. 2012. Dung beetles (Coleoptera: Scarabaeinae) attracted to Lagothrix lagotricha (Humboldt) and Alouatta seniculus (Linnaeus) (Primates: Atelidae) dung in a Colombian Amazon forest. Psyche 437589: 1-6. [ Links ]

NORIEGA, J. A.; FAGUA, G. 2009. Monitoreo de escarabajos coprófagos (Coleoptera: Scarabaeidae) en la región neotropical. pp. 165-188. En: Acosta, A.; Zapata, A. M.; Fagua, G. (Eds.). Técnicas de campo en ambientes tropicales: Manual para el monitoreo en ecosistemas acuáticos y artrópodos terrestres. Unidad de Ecología y Sistemática-UNESIS, Pontificia Universidad Javeriana, Bogotá. 215 p. https://doi.org/10.1155/2012/437589Links ]

NORIEGA, J. A.; SOLIS, C.; ESCOBAR, F.; REALPE, E. 2007. Escarabajos coprófagos (Coleoptera: Scarabaeidae) de la Provincia de la Sierra Nevada de Santa Marta. Biota Colombiana 8 (1): 77-86. [ Links ]

NORIEGA, J. A.; MORENO, J.; OTAVO, S. 2011. Quince años del arribo del escarabajo coprófago Digitonthophagus gazella (Fabricius, 1787) (Coleoptera: Scarabaeidae) a Colombia: proceso de invasión y posibles efectos de su establecimiento. Biota Colombiana 12 (2): 35-44. https://doi.org/10.21829/azm.2010.262724Links ]

NORIEGA, J. A.; SOLIS, C.; GARCÍA, H.; MURILLO-RAMO, L.; RENJIFO, J.; OLARTE, J. 2013. Sinopsis de los escarabajos coprófagos (Coleoptera: Scarabaeinae) del Caribe Colombiano. Caldasia 35 (2): 465-477. [ Links ]

NORIEGA, J. A.; CAMERO, E.; ARIAS-BURITICÁ, J.; PARDO-LOCARNO, L. C.; MONTES, J. M.; ACEVEDO, A. A.; ESPARZA, A.; MURCIA, B.; GARCÍA, H.; SOLIS, C. 2015. Grado de cobertura del muestreo de escarabajos coprófagos (Coleoptera: Scarabaeidae: Scarabaeinae) en Colombia. Revista de Biología Tropical 63 (1): 97-125. https://doi.org/10.15517/rbt.v63i1.13323Links ]

NORIEGA, J. A.; BARRANCO, W.; HERNÁNDEZ, J.; HERNÁNDEZ, E.; CASTILLO, S.; MONROY D.; GARCÍA, H. 2016. Estructura estacional del ensamblaje de escarabajos coprófagos (Coleoptera: Scarabaeinae) en una parcela permanente de bosque seco tropical. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales 40 (154): 75-83. https://doi.org/10.18257/raccefyn.255Links ]

NUNES, C. A.; BRAGA, R. F.; FIGUEIRA, J. E. C.; NEVES, F. D. S.; FERNANDES, G. W. 2016. Dung beetles along a tropical altitudinal gradient environmental filtering on taxonomic and functional diversity. Plos ONE 11 (6): e0157442. https://doi.org/10.1371/journal.pone.0157442Links ]

OSBERG, D.; DOUBE, B.; HANRAHAN, S. 1994. Habitat specificity in African dung beetles: The effect of soil type on the survival of dung beetle immatures (Coleoptera Scarabaeidae). Tropical Zoology 7: 1-10. https://doi.org/10.1080/03946975.1994.10539236Links ]

OTAVO, S. E.; PARRADO-ROSSELLI, A.; NORIEGA, J. A. 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.v61i2.11219Links ]

PEROZA, C.; DE LA OSSA, L. 1997. Situación actual del sector ganadero en el departamento de Sucre. pp. 35-37. En: Fondo Financiero de Proyectos de Desarrollo (Fonade), Fundación Futuro para Sucre, Centro de Estudios Ganaderos y Agrícolas (CEGA), Universidad de Sucre, Sincelejo. 84 p. [ Links ]

R DEVELOPMENT CORE TEAM. 2016. R: A Language and Environment for Statistical Computing. R 707 Foundation for Statistical Computing, Vienna, Available in Available in http://www.r-project.org/ . [Review date: Sep 2017]. [ Links ]

RANGEL-CH., J. O.; CARVAJAL-COGOLLO, J. E. 2012. Clima de la región Caribe colombiana. pp. 67-129. En: Rangel, J. O. (Ed.). Colombia diversidad biótica XII. La región Caribe de Colombia. Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá. 1046 p. [ Links ]

RUDAS, G.; MARCELO, D.; ARMENTERAS, D.; RODRÍGUEZ, N.; MORALES, M.; DELGADO, L. C.; SARMIENTO, A. 2007. Biodiversidad y actividad humana: relaciones en ecosistemas de bosque subandino en Colombia. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt. Bogotá D. C., Colombia. 128 p. [ Links ]

SANDERS, N. J.; RAHBEK, C. 2012. The patterns and causes of elevational diversity gradients. Ecography 35: 1-3. https://doi.org/10.1111/j.1600-0587.2011.07338.xLinks ]

SILVA, P. G. da; HERNÁNDEZ, M. I. M. 2016. Spatial variation of dung beetle assemblages associated with forest structure in remnants of southern Brazilian Atlantic Forest. Revista Brasileira de Entomologia 60: 73-81. https://doi.org/10.1016/j.rbe.2015.11.001Links ]

SILVA, R. J.; STORCK-TONON, D.; VAZ-DE-MELLO, F. Z. 2016. Dung beetle (Coleoptera: Scarabaeinae) persistence in Amazonian forest fragments and adjacent pastures: biogeographic implications for alpha and beta diversity. Journal of Insect Conservation 20 (4): 549-564. https://doi.org/10.1007/s10841-016-9885-7Links ]

SINAP (Sistema Nacional de Áreas Protegidas) 2018. Sistema de Parques Nacionales Naturales de Colombia. www.parquesnacionales.gov.co . [Review date: Sep 2017]. [ Links ]

SOLIS, A.; KOHLMANN, B. 2002. El género Canthon (Coleoptera: Scarabaeidae) en Costa Rica. Giornale Italiano di Entomologia 10: 1-68. [ Links ]

SOLIS, S.; NORIEGA, J. A.; HERRERA, G. 2011. Escarabajos coprófagos (Coleoptera: Scarabaeinae) en tres bosques secos del Departamento del Atlántico-Colombia. Boletín del Museo de Entomología de la Universidad del Valle 12 (1): 33-41. [ Links ]

SPECTOR, S. 2006. Scarabaeine dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae): an invertebrate focal taxon for biodiversity research and conservation. The Coleopterist Bulletin Monograph 5: 71-83. https://doi.org/10.1649/0010-065X(2006)60[71:SDBCSS]2.0.CO;2Links ]

TOVAR, H. L.; NORIEGA, J. A.; CARABALLO, P. 2016. Efecto de la ivermectina sobre la estructura del ensamble de escarabajos coprófagos (Coleoptera: Scarabaeidae: Aphodiinae-Scarabaeinae) en las sabanas colombianas de la región Caribe. Actualidades Biológicas 38 (105): 157-166. [ Links ]

VAZ-DE-MELLO, F. Z.; EDMONDS, W. D.; OCAMPO, F. C.; SCHOOLMEESTERS, P. 2011. A multilingual key to the genera and subgenera of the subfamily Scarabaeinae of the new world (Coleoptera: Scarabaeidae). Zootaxa 2854: 1-73. [ Links ]

VILLADA-BEDOYA, S.; CULTID-MEDINA, C. A.; ESCOBAR, F.; GUEVARA, R.; ZURITA, G. 2017. Edge effects on dung beetle assemblages in an Andean mosaic of forest and coffee plantations. Biotropica 49 (2): 195-205. https://doi.org/10.1111/btp.12373Links ]

WILLIG, M. R.; KAUFMAN, D. M.; STEVENS, R. D. 2003. Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annual Review of Ecology, Evolution, and Systematics 34: 273-309. https://doi.org/10.1146/annurev.ecolsys.34.012103.144032Links ]

Origin and funding This project was part of the B. Sc. thesis of Yina Amell-Caez at the biology program of the University of Magdalena supervised by Jorge Ari Noriega.

Suggested citation AMELL-CAEZ, Y.; DECASTRO-ARRAZOLA, I.; GARCÍA, H.; MONROY-G., J. D.; NORIEGA, J. A. 2019. Spatial diversity of dung beetle assemblages (Coleoptera: Scarabaeidae: Scarabaeinae) in five ecoregions from Sucre, Colombian Caribbean coast. Revista Colombiana de Entomología 45 (2): e7963. https://doi.org/10.25100/socolen.v45i2.7963

Received: March 30, 2018; Accepted: February 15, 2019

Corresponding author: Jorge Ari Noriega, Ph. D. Departamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias Naturales, Madrid, España. Laboratorio de Zoología y Ecología Animal - LAZOEA, Universidad de Los Andes, Bogotá, Colombia, jnorieg@hotmail.com, https://orcid.org/0000-0003-1760-7020

Author contributions

Jorge Ari Noriega and Yina Amell-Caez conceived the idea and designed the research and designed and structured the manuscript. Yina Amell-Caez gathered the data. Jorge Ari Noriega, Yina Amell-Caez, José D. Monroy-G, and Indradatta Decastro-Arrazola analyzed the data; Jorge Ari Noriega and Yina Amell-Caez wrote a first version of the paper with the help of Héctor García and Indradatta Decastro-Arrazola. All authors discussed results and approved the last version of the paper.

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License