Introduction

Scarabaeidae (Coleoptera) is one of the most studied families worldwide and particularly the beetles of the subfamily Scarabaeinae. Known as coprophagous beetles, Scarabaeinae is ecologically important because they participate in the removal and burial of manure, contributing to the aeration and fertilization of the soil (^{Nichols et al., 2007}). These dung beetles are considered an excellent focal taxon to study the response of their communities’ dynamics to habitat modifications, due to their susceptibility to changes in the structure of forest vegetation, the availability of resources and changes in environmental variables (Nichols et al., 2007).

^{Davis et al. (2004)} proposed the use of coprophagous beetles as an indicator group of habitat disturbance in tropical forests, constituting a focal group to calculate the anthropic effects concerning the alteration and fragmentation of habitats. Additionally, the Scarabaeinae has been recognized for being important indicators of the quality of ecosystems by possessing characteristics such as high diversity, functional importance, ecological fidelity and close association with other species.

The fauna of dung beetles in Colombia is represented by approximately 40 genera and about 300 species (^{Noriega et al., 2015}), which represents about 60% of the diversity of genera and 30% of Scarabaeinae species in the Neotropical region (^{Camero, 2019}).

In Colombia, most studies have focused on diversity (^{Otavo et al., 2013}; ^{Martínez-Revelo and Lopera-Toro, 2014}; ^{Martínez-Revelo et al., 2018}; ^{Amell-Caez et al., 2019}), evaluate the response to disturbances (^{Rangel-Acosta et al., 2020}), list of species for the country (^{Medina et al., 2001}) and studies on their diet (^{Bustos-Gómez and Lopera-Toro, 2003}; ^{Noriega, 2012}), but none have focused on issues relevant to the sexual ratio. ^{Fisher (1930)} postulated that the sex ratio of most species tends to be one-to-one; however, some species have been observed to deviate from this ratio, in order to maximize the evolutionary potential and long-term prospects of a population (^{Tabadkani et al., 2012}; ^{Wedekind, 2012}). In this sense, differences in the behavior of individuals, in size or morphology, are considered the main factors that may be biasing the sexual ratio in those species that present determination at the genetic level (^{Tryjanowski et al., 2009}; ^{Wedekind, 2012}).

The absence of an adequate ratio between the sexes can lead to the disappearance of a species due to the difficulty of finding a partner and therefore being able to reproduce. This is particularly important in beetles whose mating ritual is quite complex including parental care in many species (^{Escobar, 2003}).

In the Andean Amazon region, specifically in the department of Caquetá, there are no studies on gender bias in dung beetles, therefore, the main objective of this study is to test whether the populations of dung beetle species can maintain the Fisherian ratio concerning the sexes in adults and if they have any relationship with the ability to remove manure in the Parque Natural Nacional (PNN) Alto Fragua Indi Wasi.

Materials and methods

The study was carried out in the Parque Nacional Natural Alto Fragua Indi Wasi (01°17’13.3” N and 76°08’32.4” W), Vereda La Peneya, Municipality of San José del Fragua, Department of Caquetá, Colombia. The study area has an elevation of 910 meters above sea level, an average temperature of 19.9 ºC, a relative annual humidity between 85% and 90% and annual rainfall of 4,281 mm (^{Parques Nacionales Naturales, 2012}). The area corresponds to a primary forest that constitutes a corridor between the Andean and Amazonian ecosystems (^{SINCHI, 2011}).

To obtain a representative sampling of species present in the area and considering the time available in the field, a grid was established with 50 Pitfall traps baited with human fences, separated by 10 meters, to cover a total area of 5000 m2. The minimum distance between the traps and the edge of the forest was not less than 200 m. The entire system was exposed for 72 hours without interruption.

All the specimens collected during the field phase were taken to the Universidad de la Amazonia Entomology Laboratory -LEUA-, where the entomological material was separated, fixed and identified using the keys proposed by ^{Medina and Lopera-Toro (2000)} and ^{Vaz-de-Mello et al. (2011)}, under an Olympus SZ61 stereoscope and a 2x auxiliary lens. Additionally, they were sexed, measured (total length), classified into the different trophic guild and photographed using a Leica DFC450 digital camera coupled to a Leica M205A stereoscope and connected to a computer with the Leica Application Suite software, with an automatic mounting module synchronization (http://www.syncroscopy.com/syncroscopy/).

Results

In total, 693 individuals distributed in 12 genera and 26 species were collected, 407 were males (58.7%) and 286 females (41.3%), all species with Neotropical distribution (^{Medina et al., 2001}; ^{Camero and Lobo, 2010}; ^{Sarmiento-Garcés and Amat-García, 2014}; ^{Cupello, 2018}; ^{Chamorro et al., 2019a}; ^{Nunes and Vaz-de-Mello, 2019}); the most abundant species were Eurysternus cayennensis Castelnau, 1840 (n= 135 individuals, 19.5%), Dichotomius (Dichotomius) quinquelobatus (Felsche, 1910) (n= 121, 17.5%) and Eurysternus lanuginosus Génier, 2009 (n= 56, 8.1%); the less abundant species were Dichotomius (Cephagonus) fonsecae (Luederwald, 1925), Scybalocanthon sp., Canthon sp. and Sylvicanthon bridarollii (Martínez, 1949) with one individual each (0.1%) (Table 1).

The most abundant trophic guild were Diggers with 305 individuals (44%) and 14 species (53.8%), followed by the Residents with 285 individuals (41.1%) and six species (23.1%), meanwhile, the least abundant was Wheelers with 103 individuals (14.9%) and six species (23.1%) (Figure 1, Table 1). The most abundant species of the Diggers trophic guild were Dichotomius (Dichotomius) quinquelobatus (n= 121, 17.5%) and Ontherus (Caelontherus) diabolicus Génier, 1996 (n= 51, 7.4%), of the Resident group were Eurysternus cayennensis (n= 135, 19.5%) and Eurysternus lanuginosus (n= 56, 8.1%), of the Wheelers the most abundant species were Deltochilum (Deltohyboma) crenulipes Paulian, 1938 (n= 49, 7.1%) and Canthon(Glaphyrocanthon) luteicollis Erichson, 1847 (n= 33, 4.8%) (Table 1).

Figure 1 Trophic guilds of dung beetles present in the Parque Nacional Natural Alto Fragua Indi Wasi, Vereda la Peneya, San José del Fragua, Caquetá, Colombia. 

Species accumulation curve

In sampling unit four, the collection was 15 species, reaching 56.8% of the total species recorded, meanwhile for the Chao 1 and Jack 1 estimators, a concordance of 69.3% and 65.3% of the species expected was found for the same sampling unit. In sampling unit 20, 22 species were collected, reaching 84.8% of the total species, coinciding with the Chao 2 and Jack 2 estimators, which had a concordance of 88.5% and 87.5%, respectively. Finally, in sampling unit 40, 25 species were collected, corresponding to 96.5% of the total species recorded in this study, reaching a concordance of 99% and 97% according to the Chao 1 and Jack 1 estimators, which suggests that the sampling effort was ideal (Figure 2).

Figure 2 Accumulation curve of dung beetle species present in the Parque Nacional Natural Alto Fragua Indi Wasi, Vereda La Penaya, San José del Fragua, Caquetá, Colombia. 

Hill diversity index indicated that 26 species were recorded, where there are 9.8 species considered very abundant (N2=9.8) and 13.4 species considered abundant (N1=13.4), likewise the slope of the curve of the Hill index slope was not so pronounced, which is attributed to the high number of abundant and very abundant species (Figure 3).

Figure 3 Hill diversity numbers for the dung beetle species present in the Parque Nacional Natural Alto Fragua Indi Wasi, Vereda La Penaya, San José del Fragua, Caquetá, Colombia. 

Figure 4 Habitus, dorsal view, 1- Ateuchus sp. female; 2- Canthidium aff. gerstaeckeri male; 3- Canthidium aff. gerstaeckeri Harold, 1876 female; 4- Canthidium sp.1 male; 5- Canthidium sp.2 male; 6Canthidium sp.2 female; 7- Canthon luteicollis Erichson, 1847 male; 8- Canthon luteicollis Erichson, 1847 female; 9- Canthon sp. male. 

Figure 5 Habitus, dorsal view, 10- Coprophanaeus telamon (Erichson, 1847) male; 11- Coprophanaeus telamon (Erichson, 1847) female; 12- Deltochilum aff. barbipes male; 13- Deltochilum aff.barbipes female; 14- Deltochilum crenulipes Paulian, 1938 male; 15- Deltochilum crenulipesPaulian, 1938 female; 16- Dichotomius aff. inauchus male; 17- Dichotomius aff. inauchusfemale; 18- Dichotomius fonsecae (Luederwald, 1925) male. 

Figure 6 Habitus, dorsal view, 19- Dichotomius mamillatus (Felsche, 1901) male; 20- Dichotomius mamillatus (Felsche, 1901) female; 21- Dichotomius ohausi Luederwaldt, 1923 male; 22- Dichotomius quinquelobatus (Felsche, 1910) male; 23- Dichotomius quinquelobatus (Felsche, 1910) female; 24- Eurysternus caribaeus (Herbst, 1789) male; 25- Eurysternus caribaeus(Herbst, 1789) female; 26- Eurysternus cayennensis Castelnau, 1840 male; 27- Eurysternus cayennensis Castelnau, 1840 female. 

Figure 7 Habitus, dorsal view, 28- Eurysternus foedus Guérin-Méneville, 1830 male; 29- Eurysternus hypocrita Balthasar, 1939 male; 30- Eurysternus hypocrita Balthasar, 1939 female; 31- Eurysternus lanuginosus Genier, 2009 male; 32- Eurysternus lanuginosus Genier, 2009 female; 33- Eurysternus vastiorum Martínez, 1824 male; 34- Eurysternus vastiorum Martínez, 1824 female; 35- Ontherus diabolicus Génier, 1996 male; 36- Ontherus diabolicus Génier, 1996 female. 

Figure 8 Habitus, dorsal view, 37- Onthophagus sp.1 male; 38- Onthophagus sp.1 female; 39- Onthophagus sp.1 male; 40- Onthophagus sp.1 female; 41- Oxysternon silenus Castelnau, 1840 male; 42-Scybalocanthon imitans Harold, 1868 male; 43- Sylvicanthon bridarolli (Martínez, 1949) male. 

Discussion

In this study, the most abundant species were Eurysternus cayennensis, Dichotomius (Dichotomius) quinquelobatus, meanwhile, Canthon sp., Dichotomius (Cephagonus) fonsecae, Scybalocanthon sp. and Sylvicanthon bridarollii were the least abundant. These results agree with those reported by ^{Chamorro et al. (2019b)}. Dichotomius (D.) quinquelobatus, E. cayennensis and Deltochilum (Deltohyboma) crenulipes were the most abundant species of the Wheelers, Diggers and Residents trophic guilds, which also coincide with that found by Chamorro et al. (2019b).

The most abundant trophic guilds were Wheelers (Paracoprids), with 305 individuals (14 species, 53.8%), followed by Residents (Endocoprids) with 285 individuals (six species, 23.1%), meanwhile, the least abundant was Diggers (Telecoprids) with 105 individuals (six species, 23.1%). The composition of trophic guilds agrees with what was reported by ^{Basto-Estrella et al. (2012)} and ^{Chamorro et al. (2019b)} who report that in deep and slightly rocky soils and tropical humid forests, Wheelers tend to have a greater abundance. Additionally, ^{Halffter (1991)} mentions that the structure of the soil is essential to understand the diversity of Scarabaeinae since this is their habitat during much of their life cycle.

In this study, a greater abundance of males was observed, however, the Fisher test showed that there is a sexual ratio of 1.4:1 (male-female), which does not represent a significant difference over that postulated by Fisher (1930) as a 1:1 ratio, agreeing with what was obtained by ^{Barreto et al. (2021)}. However, according to ^{González-Vainer et al. (2003)} the sexual ratio varies according to the annual climatic seasonality. Additionally, ^{Onore et al. (2003)} established that the sex ratio can vary depending on the community of beetles and the locality, according to this, it must be taken into account that the biological efficacy must be stable in the ratio of males and females. In this context, differences in behavior, size or morphology must be considered as factors that may be biasing the sexual ratio in those species that present determination at the genetic level (^{Tryjanowski et al., 2009}; ^{Wedekind 2012}).

Regarding the sampling effort, the species accumulation curve showed that a 99% concordance was obtained according to the Chao 1 and Chao2 estimators and 97% and 97.8% with the Jack 1 and Jack 2 estimators, respectively. These results coincide with those recorded by ^{Ferrer-Paris et al. (2013)}, who suggests that if the number of traps is low, it will be necessary for them to work for several days, but if the number of traps is high, the effect of the sampling days is not as important as it happened with the samplings. In this study or considering more samplings at different seasonal times (high rains and low rains), the diversity of beetles could be close to 100%.

Hill diversity numbers are increasingly used for studies of diversity, taxonomy, phylogeny and trophic groups (^{Chao et al. 2014}), in this study the slope of the curve of Hill numbers reflects the unevenness of relative species abundance, the more unequal the distribution of relative abundances and the steeper the slope, the relative abundances tend to be uniform (^{Chao et al., 2016}), contrary to what was obtained in this study, where said slope does not was so pronounced, which is attributed to the high number of abundant and very abundant species.

Conclusions

Scarabaeinae is an important subfamily of beetles found in Colombia and the Amazon region, of which despite its great progress and studies, only a few ecological and taxonomic information is available for the Andean Amazon region and the department of Caquetá. This study provides relevant information on the sex ratio and habits occurrence for 12 genera and 26 species of Scarabaeinae that occur in the Parque Nacional Natural Alto Fragua Indi Wasi, San José del Fragua, Caquetá, Colombia.

The potential of dung beetles as indicators of environmental quality proposes carrying out conservation plans in the areas where they live since these individuals are important in recycling nutrients, improving soil conditions and contributing to the secondary dispersion of seeds by providing direct and indirect many ecosystem services.