Diversity of the dung beetles (Coleoptera: Scarabaeinae) in an altitudinal gradient in the east slope of los Andes, Napo province, Ecuador

ABSTRACT We present a preliminary analysis of the diversity of dung beetles in an altitudinal gradient on the East slope of Los Andes, Napo province, Ecuador. We sampled 12 localities within a 2200-m altitudinal gradient (400–2600 m a.s.l.) using pitfall traps with 2 different baits. We registered 2215 individuals distributed within 14 genera and 54 species. Ontherus pubens was the most abundant species, with registers in 10 locations that cover an altitudinal gradient of 2021 m. We also found species associated to low, medium, and high elevation levels, as well as species located on either extreme of the altitudinal gradient. The most abundant genus was Onthophagus, and the most speciose Uroxys. This survey provides 14 new registers for the Napo province and 5 novel registers for Ecuador. We present a detailed list of the species present in the Napo province with their distribution ranges, relocation guilds, and food resource preferences.


Introduction
Insects are one of the most diverse animal groups present in the tropics [1]. In the Neotropics in particular, there are areas of very high endemicity like the Amazon Region and the high mountain forests of the Andes [2,3]. Despite this great diversity and high endemicity, there are large areas that haven't been inventoried and their species richness remains unknown. This is the case for various regions in Ecuador, especially of the province of Napo for which a comprehensive list of their entomofauna is lacking [4].
Dung beetles have been extensively studied given their fundamental role in ecosystems as recyclers of the organic material produced by vertebrates, contributing to nutrient turnover in the principal biochemical cycles [27]. The majority of their species have coprophagous habits, but there are others that use different resources such as carrion, fungi, or decaying plant material [28]. Functionally speaking, there are three large guilds depending on the type of relocation of their trophic resource: tunnelers (paracoprids, which make tunnels under their trophic resource), rollers (telecoprids, who transport a portion of their trophic resource as a ball), and dwellers (endocoprids, who live within their food resource) [29]. In addition, these beetles are biological indicators in environmental impact assessment given their sensitive response to changes caused by different anthropic pressures such as deforestation, selective logging, burning, fragmentation, and hunting of mammals [27,30]. Our main objective is to describe the diversity pattern of dung beetles along an altitudinal transect in Napo province. We hypothesized a strong reduction on richness and abundance, and a replacement pattern between relocation guilds and food preferences of the dung beetles along the gradient. In addition, we present a list of the dung beetles, which constitutes new registers for the province of Napo and new registers for Ecuador.

Study site
The province of Napo, with capital in Tena (00°59′46″ S, 077°48′49″ W), is located in north-central Ecuador within the Amazon Region and presents a surface area of 13,342 km 2 ( Figure 1). The area presents a bimodal rainfall regime with two peaks, one in May-June (428 mm/ month) and the other in October (339 mm/month). Summer is in August (157 mm/month) and the annual CONTACT Jorge Ari Noriega jnorieg@hotmail.com average rainfall is of 4039 mm [31]. The altitudinal gradient ranges from 300 to 4000 m above sea level (a.s.l.) given the confluence of three bioregions: Amazon forests in low elevation areas, foothills and mountain forests in intermediate areas, and the Andean region with Andean cloud forests and paramos in high elevation areas [32]. However, the region is under an intense anthropic pressure by wood extraction and establishment of pastures for cattle and farming areas causing an increase in deforestation [33].

Data collection
From October to November 2013, a survey was performed in 12 localities covering an altitudinal gradient from 400 to 2600 m a.s.l., which was sampled every 200 m ( Figure 1). All localities were accessed through the Pan-American route following the trajectory Papallacta-Baeza-Tena-Misahualli. In each of the 12 localities, 2 parallel linear transects (separated 50 m) were established with 5 sets (separated 25 m) of 2 pitfall traps (500 ml bucket with 250 ml of soap water and separated 1 m): 1 trap containing human dung bait (15 g) and another trap with rotting fish bait (15 g) [34,35]. Overall, a total of 20 pitfall traps were placed per locality, adding up to 240 for the entire gradient. Traps were active for 48 h. The samples collected were stored in ziploc bags containing 75% alcohol and were transported to the laboratory at the National Polytechnic School (Quito-Ecuador). To identify specimens to species level, we used different taxonomical keys [5][6][7]9,10,13,36], the comparison with material deposited at the Entomological Collection of the Museum, and the assistance of taxonomical experts of this group. All samples collected were deposited (deposit code: SI-MEPN-81) in the public Entomology Collection of the "Gustavo Orces V" National History Museum within the National Polytechnic School (MEPN). Vouchers catalog number goes from MEPN 42324 to MEPN 44439.

Data analysis
For the classification of dung beetles into the three resource allocation guilds (tunnelers, rollers, and dwellers), we follow the traditional arrangement [29] associated to genus information. Food preferences groups were defined by the percentage of individuals collected in each type of bait (dung: coprophages or carrion: necrophages): when the proportion of individuals was less than 75% of one of the two baits, the species was assigned to the generalists group. We decided not to include the information related to the taxonomic level of tribe for each genus because at the moment many Neotropical genera are without tribal affiliation [37].

Results
A total of 2215 individuals distributed within 14 genera and 54 species of dung beetles were registered (Table 1). We validate our initial hypothesis, founding a strong reduction on richness and abundance and an accentuated replacement pattern between relocation guilds and food preferences of the dung beetles along the altitudinal gradient (Figure 2-4). Of all the species collected along the altitudinal gradient, we found 14 new records for the province of Napo (   Onthophagus was the most abundant genus (n = 414, 18.7%), followed by Ontherus (n = 367, 16.6%) and Deltochilum (n = 325, 14.7%). The scarcest genus was Phanaeus with only six individuals (0.3%). The most speciose genus was Uroxys (n = 8, 14.8%), followed by Canthidium, Dichotomius, Deltochilum, and Eurysternus, each one with six species. Contrariwise, four genera were represented by only one species (Coprophanaeus, Cryptocanthon, Scybalocanthon, and Sylvicanthon). The genera Oxysternon and Eurysternus disappeared rapidly along the gradient; only one species was found above 1200 m a.s.l. (Eurysternus velutinus), and only in the locality at 1376 m a.s.l. (Figure 2).
For C. cf. bicolor and Onthophagus sp. 3 that were collected on the extremities of the altitudinal gradient, we believe further revision is necessary, advocating an increased sampling effort and cryptic species verification. It is also possible that the extreme range distribution observed for these species is a result of the complex orography (i.e. steep slopes) at intermediate elevation levels within the altitudinal gradient, which complicated access and sampling at these sites.
Resource food preference groups displayed differential altitudinal distributions. Coprophages were more abundant at high levels, while necrophages were only present at specific altitudes (400, 600, and 1400 m a.s.l.) not revealing a clear pattern, and generalist species were more abundant at middle levels (1400-1600 m a.s.l.). We believe that the main food source along the altitudinal gradient is excrement, preferentially coming from  primates in low elevation areas, but supplemented by cattle excrement in high elevation areas.
We propose certain species that have a limited altitudinal range due to their association with pristine habitats as potential bioindicators for monitoring and conservation plans such as S. bridarolli, Eurysternus cayennensis, and E. caribaeus. Species like Oxysternon silenus and Coprophanaeus telamon are typically found in coffee plantations, and we propose Canthidium aff. bicolor as a species that prefers riverside habitats and swamp forests.
It is necessary to study deeply the collected material that could not be identified up to the species-level and the species that need confirmation ("cf." and "aff."), in order to finish the list for this region. Likewise, it is important to keep performing this type of studies in other localities and during different times of year, not only to complete the species inventory of Napo and Ecuador but also to understand the spatiotemporal dynamics of the altitudinal transects in the Neotropics.