In: Beetles: Biodiversity, Ecology and Role in the Environment ISBN: 978-1-63463-380-2

Editor: Camilla Stack © 2015 Nova Science Publishers, Inc.

Chapter 7

HOW A LOCALITY CAN HAVE SO MANY SPECIES?

A CASE STUDY WITH DUNG BEETLES
(COLEOPTERA: SCARABAEINAE) IN A TROPICAL
RAIN FOREST IN COLOMBIA

Jorge Ari Noriega A. 

Laboratorio de Zoología y Ecología Acuática - LAZOEA,
Universidad de Los Andes, Bogotá, Colombia

ABSTRACT
Dung beetles of the subfamily Scarabaeinae (Coleoptera: Scarabaeidae) are one of
the most important insect groups in tropical regions because their relevant ecosystem role
as organic recycling agents, biological pest controllers and secondary seed dispersers.
However, our knowledge of the different mechanisms that maintain assemblage structure
and allow species coexistence is poor. We lack such information because dung beetle
assemblages are often sampled over the short term, there are few studies that cover
extended periods of time and broad spatial areas, and it is common to use just one type of
trap and bait. To better explore the mechanisms underlying dung beetle coexistence, it
was studied a beetle assemblage found in a tropical rain forest located in Tinigua
National Park in Colombia. Sampling was conducted in August 1992, May-July and
December 1994, January and December 1995, January and July 1996, January-July 1997,
and January and July 1998. Dung beetles were sampled in the three main habitats found
in the study area: mature mainland forest, flooded lowland forest, and river beaches.
Specimens were collected using baited pitfall traps, flight interception traps, and baited
elevated traps placed at different heights using different type of baits. In addition, feces
from different vertebrates, vegetation, logs, fungi, litter, and fallen fruit were checked for
the presence of dung beetles. A total of 70 species belonging to 19 genera and 7 tribes
were collected. Compared to other areas, previously sampled in Colombia, this area
demonstrates a remarkable diversity and has a very high level of species richness (one of
the highest in the country). Nevertheless, it cannot be considered a hotspot for endemism
because there is a strong influence and contribution of species of nearby biogeographic


Email: [email protected]

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176 Jorge Ari Noriega A.

provinces to its own fauna. Some of the mechanisms that may affect the richness and
structure of the assemblage, favoring the coexistence of species are: spatial partitioning
(habitats and microhabitats), temporal partitioning (seasonality and dial activity),
resource partitioning, and guild-specific resource relocation behavior. The values of the
Jaccard similarity index reveal low levels of species overlap. Therefore, these coexistence
mechanisms appear to act in tandem to partition the ecosystem in a way that decreases
overlap among similar species, thus allowing a large number of dung beetle species to
coexist in the same area. These results demonstrate that it is necessary to carry out broad-
ranging and exhaustive sampling to fully characterize the structure of tropical dung beetle
assemblages. Finally, to completely describe the assemblage composition at this locality,
the following additional improvements should be made to the sampling protocol: carrying
out exhaustive sampling over one full year; using more specialized baits; studying the
forest canopy; searching in specialized microhabitats, such as bromeliads and ant and
termite nests; and characterizing potential phoretic interactions with mammals.

Keywords: Assemblage structure, coexistence mechanisms, Macarena, richness,

Scarabaeidae, Tinigua National Park

INTRODUCTION
The study and inventory of diverse areas is a global priority that should be supported with
as much research infrastructure as possible, especially when it comes to extremely diverse
groups that could be useful bioindicators in monitoring and conservation studies (Maguran
1988, Halffter & Favila 1993, Gaston & Hudson 1994, Hammond 1994, Myers et al. 2000).
Dung beetles of the subfamily Scarabaeinae (Coleoptera: Scarabaeidae) are one of the most
commonly used groups of insect bioindicators because of the important ecological roles they
play (Nichols et al. 2008). Adults and larvae feed on dung produced by mammals, thus
helping to recycle organic matter (Halffter & Matthews 1966, Howden & Young 1981,
Halffter & Halffter 1989, Gill 1991). Besides this function, dung beetles act as parasitic
controllers of flies and nematodes (Waterhouse 1974) and also as secondary seed dispersers
(Estrada & Coates 1991, Andresen 2001).
Among the countries located in the Neotropics, Colombia has one of the highest levels of
dung beetles diversity. Knowledge about this group has been growing over the last two
decades thanks to the publication of several important articles (Escobar & Medina 1996,
Amat et al. 1997, Amezquita et al. 1999, Escobar 2000, Medina et al. 2001, 2002, Escobar
2004, Escobar et al. 2005, Fuentes & Camero 2006, Noriega et al. 2007, Martinez et al. 2009,
Giraldo et al. 2011, Solis et al. 2011, Cultid et al. 2012, Delgado-Gómez et al. 2012, Noriega
et al. 2012, Otavo et al. 2013). However, some of these studies cover only short time periods
of sampling and use only a few different types of traps, frequently with just one kind of bait,
which means that they are little more than rapid surveys of biodiversity; consequently, they
provide an incomplete characterization of dung beetle assemblage richness.
In ecological classic literature is commonly assumed that the dynamic of the structure of
an assemblage is influenced mainly by interspecific competition of a limiting resource in
space and time, affecting the coexistence of more then two species (Hairston et al. 1960,
Levins & Culver 1971, Hastings 1980, Tilman 1980, Atkinson & Shorrocks 1981, Connor &
Simberloff 1983, Schoener 1983). Following the principal of competitive exclusion, two

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 How a Locality Can Have so Many Species? 177

species cannot occupy the same ecological niche and if the resource they share is a limiting
factor one of them will exclude the other one (Hardin 1960). In this sense, several studies
with dung beetles have found that competition is an important factor that affects the
composition, richness and abundance in assemblages (Hanski 1981, Holter 1982, Peck &
Forsyth 1982, Giller & Doube 1989, Hanski & Cambefort 1991, Giller & Doube 1994,
Montes de Oca & Halffter 1995, Hirschberger 1998, Krell-Westerwalbesloh et al. 2004, Feer
& Pincebourde 2005, Horgan 2005, Horgan & Fuentes 2005, Vernes et al. 2005, Horgan
2006, Hernández et al. 2011). However, there is so few information that characterizes the
mechanisms that support the coexistence in rich-species assemblages localities.
This study aimed to provide greater insight into this group by conducting a complete
species inventory at one of the most biologically interesting areas in the country (Noriega
et al. 2015). The study‘s main question was the following: how can a given area support such
a large number of species? The goal was also to understand the coexistence mechanisms
operating in the dung beetles assemblage that minimize interspecific competition, including
spatial, temporal, and resource partitioning as well as resource relocation behavior.

MATERIALS AND METHODS

Study Area

The study was carried out at the Center for Ecological Research of La Macarena (Spanish
abbreviation: CIEM); the study area (2º40‘ N - 74º10‘ W, 350-400 m.a.s.l.; Figure 1) was
situated in a tropical rainforest found to the west of the Duda river, 13 km upstream from the
Duda‘s junction with the Guayabero, and located near the eastern border of Tinigua National
Park (201.875 ha; Meta Department, Colombia). The park was created in 1989 to establish a
biological corridor between the parks of La Macarena and Picachos. The Serrania of La
Macarena is part of the biogeographic province of the Guayana presenting a complex mosaic
of faunal and floral elements (Hernandez et al. 1992).
The region is characterized by a high degree of seasonality (Kimura et al. 1994). The dry
season lasts from December to March, and rainfall varies the rest of the year (>100 mm per
month). Average annual rainfall is 2600 mm; monthly rainfall is lowest in January (as low as
0 mm) and highest in May (up to 530 mm). Average annual temperature is 25°C (Kimura et
al. 1994). The area has soils with different and complex geological origins. They were largely
created by Plio-Pleistocene alluvial plates, experiencing recent tectonic fracturing and water
erosion; consequently, they have low fertility and a poor cationic exchange capacity, are
oligotrophic and deficient in mineral elements (Hirabuki 1990).
Sampling was carried out in the study area‘s three main habitats (described by Hirabuki
1990; Figure 2):

- Mature mainland tropical rain forest (MF): primary tropical rainforest with a
continuous canopy containing trees of 25–30 m and emergent trees that reach 35 m.
This type of forest is associated with the highest diversity of tree species (Barbosa &
Hirabuki 1992) and has the highest vegetative cover in the area (53%) (Hirabuki
1990, Stevenson et al. 2004).

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178 Jorge Ari Noriega A.

- Flooded lowland tropical rain forest (FF): lowland forest located on flatlands that are
partially flooded during the rainy season by the river. It has a discontinuous canopy
that is dominated by Ficus spp., Inga spp., and Cecropia sp. and an underbrush that
contains mainly Heliconia spp. In this area, vegetative cover is 11% in this type of
forest (Hirabuki 1990).
- River beaches (RB): beaches located on the banks of the Duda river. Their number
and size vary throughout the year depending on rainfall seasonality. During the rainy
months, the river increases in volume and covers the beaches completely within a
few days. In the dry season, the beaches reappear, although the river never dries up
completely. During the dry months, sand surface temperatures reach 50–55°C. These
beaches are characterized by a type of early successional riparian forest containing
Tessaria integrifolia and young trees of Cecropia sp.

Figure 1. Geographical location of the study area: CIEM - Tinigua National Park, Meta Department,
Colombia.

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 How a Locality Can Have so Many Species? 179

Figure 2. Habitats sampled at CIEM - Tinigua National Park, Meta Department, Colombia. A) Mature
mainland tropical rain forest - MF, B) Flooded lowland tropical rain forest – FF and C) River beaches –
RB.

In terms of vertebrates this area is a diverse spot with high species richness in different
orders as Artiodactyla (3 spp.), Carnivora (9 spp.), Lagomorpha (1 sp.), Perissodactyla (1 sp.),
Rodentia (6 spp.) and Xenarthra (5 spp.) (Stevenson 2002). In addition, it is home to seven
coexisting species of primates: Lagothrix lagothricha (Humboldt, 1812 – common woolly
monkey), Sapajus apella (Linnaeus, 1758 - brown capuchin), Ateles belzebuth Geoffroy,
1806 - spider monkey, Alouatta seniculus (Linnaeus, 1766 - red howler monkey), Saimiri
sciureus (Linnaeus, 1758 - squirrel monkey), Callicebus cupreus (Spix, 1823 - red titi) and
Aotus brumbacki Hershkovitz, 1983 - brumback´s night monkey (Stevenson 2002). Woolly
monkeys and howler monkeys have the highest densities and levels of biomass (Stevenson &
Quiñones 1993).

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180 Jorge Ari Noriega A.

Dung Beetles Sampling, Data Review and Food Relocation Guilds

The author collected specimens in the habitats described above between June to July
1994, December 1994 to January 1995, December 1995 to January 1996, as well as in July
1996 and January 1998. Besides, other researchers studying dung beetles in the same area
also collected some samples (from January to July 1997 and in July 1998) that were included
in the analyses. In addition, it was included data from specimens that were found while going
through the review of the largest entomological collections in Colombia: Entomological
Collection Instituto Alexander von Humboldt (IAvH), Entomological Collection Instituto de
Ciencias Universidad Nacional de Colombia (ICN-MHN), Entomological Collection
Universidad de Antioquia (CEUA), Entomological Collection Universidad del Cauca (MHN-
UC), Entomological Collection Pontificia Universidad Javeriana (MPUJ), Entomological
Collection Universidad de Nariño (PSO), Entomological Collection Universidad de Tunja
(CCM-FM) and Entomological Collection Natural History Museum of Universidad de Los
Andes (EANDES). These collections contain some specimens that were collected during
some of the same time periods as those mentioned above as well as some specimens collected
in August 1992 and May 1994. Furthermore, data were added from any published reports or
studies for which dung beetles in this area were sampled (Castellanos et al. 1999, Laverde et
al. 2002, Noriega 2002b, 2004, Noriega & Calle 2008, Noriega 2011, Noriega & Acosta
2011, Noriega 2012).
Specimens were collected using pitfall trap arrays (Noriega & Fagua 2009); traps were
baited with human excrement, carrion (rotten fish, squid, calamari, and chicken), or fruit
(banana) and were left at least 48 hours (20160 hours/traps; Noriega et al. 2005). Flight
interception traps were also used. Arrays of elevated traps placed at different heights were
baited with human excrement, rotten fish, mushrooms, and decaying fruit (Noriega, unpubl.
data). Additionally, dung from different vertebrates—such as L. lagothricha, A. seniculus,
Hydrochaeris hydrochaeris (Linnaeus, 1766) (capybara), Crocodylus intermedius (Graves,
1819) (Orinoco crocodile), and Tapirus terretris (Linnaeus, 1758) (brazilian tapir)—was
visually inspected for the presence of beetles. In addition, individuals were manually
collected from vegetation, logs, flowers, fungi, leaf litter, and fallen fruit along the CIEM‘s
trail system.
All specimens were preserved in 70% ethanol upon collection. They were later dried and
identified to species using different taxonomic keys (Halffter & Martinez 1977, Howden &
Young 1981, Kohlmann 1984, Jessop 1985, Edmonds 1994, Genier 1996, Kohlmann & Solis
1997, Cook 1998, Edmonds 2000, Medina & Lopera 2000, Kohlmann & Solis 2001, Solis &
Kohlmann 2002, Edmonds & Zidek 2004, Solis & Kohlmann 2004, Kohlmann & Solis 2006,
Vaz-de-Mello 2008, González et al. 2009, Camero 2010, Edmonds & Zidek 2010, Molano &
Medina 2010, Vaz-de-Mello et al. 2011, Cupello & Vaz-de-Mello 2013, Solis & Kohlmann
2013), reference specimens in entomological collections, and the assistance of taxonomic
experts. A reference collection was deposited at the EANDES in Bogotá, Colombia, and
specimens from almost all the species collected were distributed to various entomological
collections in Colombia: IAvH, ICN-MHN, and Universidad Pedagógica Nacional
(MHNUPN). Specimens were also placed in the personal reference collections of Alejandro
Lopera (CAL) and the author (CJAN).
Dung beetles food-relocation groups incorporated in the analysis where defined using the
guilds described by Bornemissza (1976) and Halffter & Edmonds (1982): paracoprids (T,

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 How a Locality Can Have so Many Species? 181

tunnelers)—species that dig a vertical tunnel below the food resource and transport a fraction
of it into the bottom of the burrow to build their nests; telecoprids (R, rollers)—species that
make a ball from the resource, roll it horizontally and later bury it into the ground building a
nests; and endocoprids (D, dwellers)—species that occur within the food resource and make
their nests there or in the interphase soil – resource. Since, for some species, it was impossible
to directly observe specific relocation behaviors in the field, the distinctive behavior of the
genus was assumed to occur.
In addition, the beetles were placed in three researcher-defined size categories: small
(<10 mm), medium (10–18 mm) and large individuals (>18 mm). This was an adaptation of
the system proposed by Doube (1990).

Data Analysis

An Excel matrix was constructed using the information on the niche characteristics of all
of the 70 species sampled (habitat, season, dial activity, resource preferences, and guild-
resource relocation behavior). These niche characteristics (coded as 14 grouped binomial
variables placed in 6 ecological categories) were transformed into orthogonal components by
performing a principal coordinates analysis on a matrix of Jaccard similarities. The five first
components that accounted for more than 5% of the variability of the original matrix (70
species x 14 variables) and that, in addition, fulfilled the ―broken stick‖ criterion were
retained (Peres-Neto et al. 2006). Ecological patterns were interpreted by examining the five
components obtained and comparing the positions of each species in each component based
on the variable states (0-1); for each component, variables were selected using ANOVAs
(p<0.001).
Using all of the species positions (derived from the principal coordinates analysis), a
matrix of the Euclidean distances between the different pairs of species was obtained. Using
this new matrix, it was possible to calculate the overall average distance between species as
well as the average of the top 1% of distances between species (C70,2=2415). These two
measurements reveal the average and maximum degree of ecological divergence between
species, respectively.
The matrix of 70 species x 5 components, which defined the ecological niches of the
species in the study area, was used to generate 9999 neutral matrices of the ―ecological
positions‖ of the species. The neutral positions of the 70 species in each of the five orthogonal
components were determined by randomly redistributing the values of the species within each
component; consequently, because species values were not correlated across components, it
was ensured that the different components would not be related (i.e., r0).
These neutral matrices had the same dimensions (70 x 5) and contained the same amount
of information as the original matrix of observed values. However, because they described
randomly generated species, whose niches were not determined by real-life interspecific
ecological interactions, they served as controls that could be used to determine if the observed
degree of ecological packing was greater or less than what would be expected according to a
neutral model based on random distributions. The overall average distance between the 70
species as well as the average of the top 1% of distances between species were calculated for
each of the 9999 neutral matrices.

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182 Jorge Ari Noriega A.

These values were used to build two distributions, which revealed whether the observed
average and maximum degrees of species divergence were greater or smaller than what would
be expected by chance. In addition, a species similarity analysis based on the Jaccard index
was performed using all the ecological characteristics examined. All the analyses were done
using the free statistical software packages PAST (v. 3.02, 2014; Hammer et al. 2001) and
PopTools (v. 3.2; Hood 2010).

RESULTS AND DISCUSSION

Assemblage Structure
A total of 70 species—belonging to 19 genera and 7 tribes—were collected (Table 1,
Figure 3). In terms of species richness, the dominant genus in the area was Dichotomius
(11 species), followed by Canthon (9 species) and Canthidium (8 species). The most
abundant species in the region were O. haematopus, C. cupreum, C. aequinoctialis, D. parile,
and O. conspicillatum; they were the most commonly sampled species in both this study and
some other studies conducted in the area (Castellanos et al. 1999). It is particularly interesting
to note that S. leander and G. lemoinei were present; they are the only two species found on
river beaches (Figure 3; Noriega 2002).

Table 1. List of the species of dung beetles (Scarabaeinae) collected at the CIEM -
Tinigua National Park, Meta Department, Colombia. Code Spp: species code

Tribe Species Code Spp.

Ateuchini Ateuchus murrayi (Harold, 1868) Ate mur

Ateuchus pygidialis (Harold, 1939) Ate pyg
Ateuchus cf. scatimoides (Balthasar, 1939) Ate sca
Eutrichillum cf. hirsutum (Boucomont, 1928) Eut hir
Uroxys bidentis Howden & Young, 1981 Uro bid
Uroxys micros Bates, 1887 Uro mic
Uroxys sp. 1 Uro sp1
Uroxys sp. 2 Uro sp2
Coprini Canthidium euchalceum Balthasar, 1939 Can euc
Canthidium funebre Balthasar, 1939 Can fun
Canthidium gerstaeckeri Harold, 1867 Can ger
Canthidium onitoides (Perty, 1830) Can oni
Canthidium ruficolle (Germar, 1824) Can ruf
Canthidium splendidum Preudhomme de Borre, 1886 Can spl
Canthidium cf. centrale Boucomont, 1928 Can cen
Canthidium cf. cupreum (Blanchard, 1845) Can cup
Dichotomius belus (Harold, 1880) Dic bel
Dichotomius boreus (Olivier, 1789) Dic bor
Dichotomius compressicollis (Luederwaldt, 1929) Dic com
Dichotomius deyrollei (Harold, 1869) Dic dey
Dichotomius mamillatus (Felsche, 1901) Dic mam
Dichotomius ohausi (Luederwaldt, 1923) Dic oha

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 How a Locality Can Have so Many Species? 183

Tribe Species Code Spp.

Dichotomius podalirius (Felsche, 1901) Dic pod
Dichotomius worontzowi (Pereira, 1942) Dic wor
Dichotomius cf. problematicus (Luederwaldt, 1922) Dic prb
Dichotomius cf. protectus (Harold, 1867) Dic prt
Dichotomius aff. inachus (Erichson, 1847) Dic ina
Ontherus azteca Harold, 1869 Ont azt
Ontherus pubens Génier, 1996 Ont pub
Deltochilini Canthon aequinoctialis Harold, 1868 Can aeq
Canthon angustatus Harold, 1867 Can ang
Canthon cyanellus Harold, 1863 Can cya
Canthon femoralis (Chevrolat, 1834) Can fem
Canthon fulgidus Redtenbacher, 1867 Can ful
Canthon lituratus (Germar, 1813) Can lit
Canthon luteicollis Erichson, 1847 Can lut
Canthon mutabilis Lucas, 1859 Can mut
Canthon cf. gutierrezi Martínez, 1950 Can gut
Deltochilum amazonicum Bates, 1887 Del ama
Deltochilum orbiculare van Lansberge, 1874 Del orc
Deltochilum aff. orbignyi (Blanchard, 1845) Del org
Deltochilum aff. parile Bates, 1887 Del par
Scatonomus cf. insignis Harold, 1867 Sca ins
Scybalocanthon pygidialis (Schmidt, 1922) Scy pyg
Scybalocanthon cf. imitans (Harold, 1868) Scy imi
Demarziellini Bdelyrus cf. metaensis Cook, 1998 Bde met
Oniticellini Eurysternus caribaeus (Herbst, 1789) Eur car
Eurysternus contractus Génier, 2009 Eur con
Eurysternus foedus Guérin-Méneville, 1844 Eur foe
Eurysternus hamaticollis Balthasar, 1939 Eur ham
Eurysternus hypocrita Balthasar, 1939 Eur hyp
Eurysternus mexicanus Harold, 1869 Eur mex
Eurysternus plebejus Harold, 1880 Eur ple
Eurysternus wittmerorum Martínez, 1988 Eur wit
Onthophagini Onthophagus buculus Mannerheim, 1829 Ont buc
Onthophagus haematopus Harold, 1875 Ont hae
Onthophagus rubrescens Blanchard, 1845 Ont rub
Onthophagus cf. curvicornis (Latreille, 1811) Ont cur
Onthophagus aff. clypeatus Blanchard, 1846 Ont cly
Phanaeini Coprophanaeus telamon (Erichson, 1847) Cop tel
Coprophanaeus ohausi (Felsche, 1911) Cop oha
Dendropaemon cf. waterhousei d´Olsoufieff, 1924 Den wat
Gromphas lemoinei Waterhouse, 1891 Gro lem
Oxysternon conspicillatum (Weber, 1801) Oxy con
Oxysternon silenus Castelnau, 1840 Oxy sil
Phanaeus bispinus Bates, 1868 Pha bis
Phanaeus cambeforti Arnaud, 1982 Pha cam
Phanaeus chalcomelas (Perty, 1830) Pha cha
Sulcophanaeus faunus (Fabricius, 1775) Sul fau
Sulcophanaeus leander (Waterhouse, 1891) Sul lea

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184 Jorge Ari Noriega A.

One of the least common species was S. faunus: it never came to baited pitfall traps, even
those baited with carrion (rotten fish, squid, calamari, and chicken). The only two individuals
that were collected (one male and one female) were captured in a mist net intended for birds.
It is also interesting to note that individuals of the genus Ontherus (O. azteca and O. pubens)
occurred in low numbers. Genier (1996) says that some species of this genus have very
specific habitat restrictions and resource preferences that may explain these low numbers.
For instance, in the study area, there are ant and termite nests that could serve as
microhabitats for these two species (Kistner 1982, Krikken 2008, Krell & Phillips 2010,
Vårdal & Forshage 2010, Maruyama 2012), which may explain why O. azteca was frequently
observed in interception traps. Other species that also occurred in low numbers were
Scatonomus cf. insignis, Bdelyrus cf. metaensis, and Eutrichilum cf. hirsutum; little
information is available on the ecology, behavior, and habitat preferences of these three
genera (Pereira 1954, Martínez 1967, Vulcano & Pereira 1973, Ratcliffe 1980, Cook 1998,
Medina et al. 2001, Solis et al. 2011).

Table 2. Different numbers of Scarabaeinae found in five biogeographical regions in

Colombia (Ama: Amazon, And: Andean, Car: Carribean, Cho: Choco – Pacific,
Ori: Orinoquia – Plain grasslands and Guy: Guayana) and at the CIEM - Tinigua
National Park, Meta Department, Colombia

Altitude Genera/
Region Department Locality Reference
(m.a.s.l.) Species

Amazonas Leticia 80 15/60 Howden & Nealis (1975)

Ama
PNN Serranía de
Caquetá 300 14/61 Pulido et al. (2003)
Chiribiquete
160, 2600
Caldas Cuenca Río La Miel 12/55 Arango & Montes (2009)
And - 2750
Tolima Mariquita 690 13/30 Fuentes & Camero (2006)
Atlántico Barranquilla 0 - 500 17/35 Solís et al. (2011)
Car PNN Sierra Nevada de
Magdalena 50 - 940 15/29 Martínez et al. (2009)
Santa Marta
Choco Salero 115 13/23 Neita et al. (2003)
Cho
Choco Lloro 90 13/19 Neita & Escobar (2011)
Meta Puerto Colombia 200 14/32 Amézquita et al. (1999)
Ori San José del Guaviare,
Guaviare 200 - 360 14/48 Escobar (2000)
RN Nukak
Guy Meta CIEM 350 19/70 (this work)

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Figure 3. Dorsal view of a sample of dung beetle species in the CIEM - Tinigua National Park, Meta
Department, Colombia. a) Onthophagus haematopus (♀), b) Eurysternus plebejus (♂), c) Canthidium
funebre (♀), d) Scybalocanthon pygidialis (♀), e) Canthon luteicollis (♀), f) Canthon aequinoctialis
(♂), g) Canthon fulgidus (♂), h) Eurysternus caribaeus (♀), i) Phanaeus chalcomelas (♂), j)
Dichotomius belus (♂), k) Gromphas lemoinei (♂), l) Eurysternus hamaticollis (♂), m) Coprophanaeus
telamon (♂), n) Oxysternon conspicillatum (♂), o) Sulcophanaeus leander (♂), p) Deltochilum orbignyi
(♀), q) Sulcophanaeus faunus (♂). Bar scale = 1 cm.

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186 Jorge Ari Noriega A.

If species richness in this area is compared with that in other parts of Colombia, the area
around the CIEM is one of the most species rich in the country (Noriega et al. 2015; Table 2).
Given the high number of species it shares with neighboring biogeographical regions (n=56;
79.8%) and its low number of endemic species (n=4; 5.7%) compared to other areas of the
country (Escobar 2000), faunal composition in this area is likely greatly determined by
species contributions distributed in the entire country (n=8; 11.4%), in surrounding regions
(Andes, Amazonia, and Orinoquia) and less influenced by local speciation (i.e., inside the
Guayana region, agreeing with the proposed by Hernandez et al. 1992) (Figure 4).

Figure 4. Composition of dung beetle species assemblage at the CIEM - Tinigua National Park, Meta
Department, Colombia, in terms of the species biogeographical origin: Endemic (1), Andes (2),
Orinoquia (3), Amazonia (4) or present throughout the entire country.

Spatial Coexistence Mechanisms

Taxonomic richness was highest in MF, which harbored 17 genera, 53 total species
(75.7%), and 41 unique species (58.6%). Next was FF with 12 genera, 28 total species (40%),
and 15 unique species (21.4%). Last were the RB with just 2 genera, 2 total species (2.9%),
and 1 unique species (S. leander). There are no species that were present in all the CIEM‘s
main habitats. However, MF and FF shared 13 species (18.6%), and FF and the RBs shared
just one species (G. lemoinei) (Figure 5).
Vertical partitioning of forest habitat appears to be another important spatial coexistence
mechanism. Given the results obtained from the linear transect of elevated traps (Noriega
2011) placed at heights of 3, 6, 9, and 15 m in MF, it is clear that some species are using
different strata within the forest (floor - 0 m vs. arboreal level – 6 m) and are especially
abundant between 6 and 9 m (Noriega unpub. data). Of the 70 species found in this area, 10

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(14.7%; B. cf. metaensis, C. funebre, C. gerstaeckeri, C. cf. cupreum, C. aequinoctialis, C.

fulgidus, C. luteicollis, O. buculus, O. haematopus and S. pygidialis) came to the elevated
traps.
In particular, B. cf. metaensis was collected exclusively in one such trap, and C. fulgidus
was by far more common in traps located 6 m above the ground than in ground-level pitfall
traps. Other species like C. splendidum, C. angustatus, and O. conspicillatum were found
perching on leaves in the forest but never occurred in the elevated traps (Noriega unpub.
data). It is recommended to install elevated traps in the canopy and studying this as yet
unexamined stratum of the forest; it is possible that some species use the canopy
microhabitat.

Figure 5. Shared and unique species in the three main habitats (MF=Mature mainland forest,
FF=Flooded lowland forest and RB=River beaches) of the CIEM - Tinigua National Park, Meta
Department, Colombia.

Temporal Coexistence Mechanisms

The wet season was more taxonomically rich (17 genera; 57 total species, 81.4%, 60.2%
in contrast; 32 unique species, 45.7%) than the dry season (13 genera; 38 total species, 54.3%,
39.8% in contrast; 13 unique species, 18.6%; Figure 6). Twenty-five species (35.7%)
occurred during both seasons. However, sampling during the transition season was
incomplete, and it is certain that there are no species that were present throughout the entire
year at the CIEM. It is noteworthy that five of the eight species of the genus Eurysternus were
present during both seasons. In general, the arrival of the rainy season produces an increase in
resources in the forest that favors the coexistence of a greater number of species; the opposite
occurs during the dry season, as it was registered in other studies (Montes de Oca & Halffter
1995, Morelli et al. 2002, Vernes et al. 2005).

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188 Jorge Ari Noriega A.

As for dial activity, slightly more species were out during the day (14 genera; 40 total
species, 57.1%, 52.4% in contrast; 31 unique species, 44.3%) than at night (13 genera, 39
total species, 55.7%, 47.6% in contrast; 30 unique species, 42.9%; Figure 6). Nine species
(12.9%) occurred both during the day and at night hours. However, no species was active all
day (24 hours), and most had very short windows of activity during the crepuscular hours—
for instance, S. leander is active for less than an hour at dusk and dawn (Noriega 2002b).
These differences in periods of activity decrease the competition for limited resources in dung
beetles (Hanski & Cambefort 1991, Estrada et al. 1993, Giller & Doube 1994, Montes de Oca
& Halffter 1995, Hernández 2002, Krell-Westerwalbesloh et al. 2004).
This crepuscular peak in activity is probably related to the fact that mammals, and
especially primates, produce much more dung at dawn and during the early morning, as it has
been registered for L. lagotricha in this locality, after one hour of rest (P. Stevenson pers.
comm.). During the middle of the day (12–2 pm) and after the middle of the night (12–2 am),
species number and activity are lower (Noriega unpub. data). In addition, it is possible that
some species prefer resources in a specific state of decay or freshness (e.g., fresh vs. old;
Hanski 1980b); such preferences have yet to be studied in this area.

Figure 6. Structure of the dung beetle assemblage found at the CIEM - Tinigua National Park, Meta
Department, Colombia. Four different categories of niche partitioning were examined: season (wet vs
dry), resource preference (dung vs carrion), dial activity (day vs night) and resource-relocation behavior
(tunnelers vs rollers vs dwellers).

Resource Coexistence Mechanisms

More species were found on dung (19 genera; 63 total species, 90%, 84.2% in contrast;
58 unique species, 82.9%) than on carrion (7 genera; 12 total species, 17.1%, 15.8% in
contrast; 7 unique species, 10%; Figure 6). Five species (7.1%) occurred on both resources
(C. aequinoctialis, C. telamon, D. amazonicum, E. caribaeus and E. plebejus), which show

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 How a Locality Can Have so Many Species? 189

that they are generalists in terms of their food preferences. The differences in the spatial
distributions and abundances of these two resources have a clear effect on the number of
species associated with each. The high richness and abundance of dung beetles in this area is
supported by the high diversity and density of mammals. Castellanos et al. (1999) estimated
that woolly monkey populations in this area might produce 400–600 fecal deposits/km2 per
day. However, this study found that a large number of species use carrion, a result that
contrasts with those of other studies in Colombia (Howden & Nealis 1975, Bustos-Gómez &
Lopera 2003, Pardo et al. 2004, Esparza-Leon & Amat-García 2007, Murillo et al. 2010,
Delgado-Gomez et al. 2012) and in other regions (Hanski 1983, Klein 1989, Hill 1996,
Boonrotpong et al. 2004, Larsen et al. 2006, Damborsky et al. 2008, Almeida & Louzada
2009, Davis et al. 2010, Barragan et al. 2011). The exploitation of carrion could be related to
the Neotropical absence of large mammals (Halffter & Matthews 1971, Louzada & Lopes
1997), which can produce large quantities of excrement; consequently, some species of dung
beetles may have turned to other available resources.
In addition, some studies in Colombia (Santos-Heredia et al. 2010) and in other regions
(Howden & Young 1982, Estrada & Coates 1991, Gill 1991, Estrada et al. 1993) suggest that
dung beetles might be highly specialized in the type of mammal excrement (carnivorous,
herbivorous or omnivorous) they use. Another study conducted in this area (Noriega 2012)
compared species preferences for excrement produced by two different primates (A. seniculus
and L. lagotricha); it found that some beetle species were more attracted to the dung produced
by one primate and not to that produced by the other. It is also important to note that most of
the baits used in this study were small in size (20–30 g), and it is possible that some species
could be more attracted to smaller or larger baits (Gill 1991). For instance, based on data
obtained in other areas and from the literature (Edmonds & Zidek 2010), it is proposed that S.
faunus is not attracted to small baits but rather prefers large carcasses in highly conserved
forests.
Furthermore, numerous records show that some dung beetles use other, very specific
resources that are completely different from vertebrate dung and carrion, such as invertebrate
feces, flowers, fungi, fruits, eggs, and diplopods, among others (Young 1980, Monteith &
Storey 1981, Howden & Young 1982, Gill 1991, Navarrete & Galindo 1997, Cano 1998,
Pfrommer & Krell 2004, Noriega & Calle 2008, Halffter & Halffter 2009). The fact that these
species exploit such a wide range of non-fecal resources raises the question as to whether this
group of insects should even be called ―dung beetles‖ at all.

Guild-Resource Relocation Coexistence Mechanisms

In terms of the dung beetle guilds that show resource relocation behavior, the paracoprids
(T) were the most common (14 genera; 46 species, 63.9%), followed by the telecoprids (R) (4
genera; 16 species, 25.0%) and the endocoprids (D) (1 genus, Eurysternus; 8 species, 11.6%;
Figure 6). Some additional resource relocation behaviors were observed at the CIEM, such as
pellet- or fragment-pushing, but they were exhibited by very few species and not commonly.
If beetle size (small, medium and large) is examined in tandem, it is possible to gain a
better idea of how effectively relocation behavior limits direct competition and partitions
species in this area. Indeed, the results indicate that, in some categories like medium and
small rollers and large, medium, and small dwellers, there were no more than three species

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190 Jorge Ari Noriega A.

sharing the resource (Table 3). No kleptoparasitism was directly observed in the field in this
area, but since this behavior is very common at other localities (Cambefort 1991, Gill 1991,
Rougon & Rougon 1991), it seems highly probable that it occurred between small and large
species.

Table 3. Matrix of beetle species belonging to different resource-relocation guilds

(tunnelers, rollers and dwellers) and of different sizes (large, medium and small) found
at CIEM - Tinigua National Park, Meta Department, Colombia

TUNNELERS ROLLERS DWELLERS

Cop tel Dic wor Del ama Eur con
Cop oha Oxy con Del orc Eur ham
LARGE
Dic bor Sul fau Del org Eur hyp
(> 18 mm)
Dic mam Sul lea
Dic pod
Can cen Dic prb Can aeq Eur car
Can ful Gro lem Eur foe
Den wat Ont pub
Dic bel Ont azt
MEDIUM
Dic com Oxy sil
(10 – 18 mm)
Dic dey Pha bis
Dic ina Pha cam
Dic oha Pha cha
Dic prt
Ate mur Eut hir Can ang Can mut Eur mex
Ate pyg Ont buc Can cya Del par Eur ple
Ate sca Ont cly Can fem Sca ins Eur wit
Can cup Ont cur Can gut Scy pyg
Can euc Ont hae Can lit Scy imi
SMALL
Can fun Ont rub
(< 10 mm)
Can ger Uro bid
Can lut Uro mic
Can oni Uro sp1
Can ruf Uro sp2
Can spl Bde met

Ecological Segregation of Species

The five components retained in the principal coordinates analysis accounted for 71% of
the interspecific variability in species niche characteristics. The first component (Table 4)
accounted for 27.76% of the niche information (species that were found in MF, active during
wet season, with nocturnal activity and they use carrion resources).
The second component included the 20.57% of the niche (species that were found in FF,
active during dry season, with nocturnal activity and with paracoprid behavior). These two
components alone accounted for nearly the 50% of the ecological divergence between
species. The third, fourth, and fifth components, which explained the 22.9% of the variability,
are described in Table 4. Based on these five components, the average degree of divergence

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 How a Locality Can Have so Many Species? 191

between species was 0.363 (the maximum theoretical value is 1, and the maximum observed
Euclidean distance was 0.723).

Table 4. Analysis of the principal coordinates matrix for all the species sampled at
CIEM - Tinigua National Park, Meta Department, Colombia. The signs + and –
indicates respectively, the positive and negative relationships that exist between the
binomial variables (0-1), which describe the species niche characteristics and the five
principal coordinates components

Comp 1 Comp 2 Comp 3 Comp 4 Comp 5

MF + - -
FF - + - -
RB
Dry - + - - -
Wet + - + -
Day - - + -
Night + + - +
Dung - + +
Carrion + - -
Tunneler + + - +
Roller - +
Dweller -
Floor - - +
Arboreal + +
Autovalue 3.90 2.89 1.49 0.94 0.79
% variance 27.76 20.57 10.60 6.71 5.59

This observed average value was significantly greater than the average of the neutral
distribution (P=0.050; Figure 7). This result means that the 70 species sampled were slightly
more segregated than expected by chance based on a neutral model of ecological segregation.
In contrast, average maximum divergence was significantly smaller (p=0.036; Figure 7) than
expected by chance (neutral model: average maximum value of 0.970). This result indicates
that there are no extreme ecological positions within the niche space of the group of species
and therefore not observed degrees of ecological segregation that did not have representation
in the 70 species registered.
On average, species were more ecologically segregated than expected by chance, but
species with extreme ecological niches were not detected, which generated maximum values
of interspecific divergence within the niche space available for the 70 species.

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192 Jorge Ari Noriega A.

Figure 7. Euclidian average and maximum distance between pair of species sampled at the CIEM -
Tinigua National Park, Meta Department, Colombia.

The analysis of similarity using Jaccard index shows that there are 20 different groups of
species or single species with a 75% of similarity (25% of dissimilarity) that do not use and
share the niche in the same way (Figure 8).
Relative to the high level of species richness in this area, the degree of interspecific niche
overlap is low, meaning that few species interact directly in the same space, at the same time,
and on the same resource (Figure 9). Indeed, this assertion is supported by the presence of all
of the coexistence mechanisms described above.
If the information of food relocation guilds and categories of size (Table 3) is added with
the coexistence scheme of niche segregation structure (Figure 9) there were very few species
sharing the same space, time and resource decreasing radically the interspecific competition.
In addition, it is important to notice that at least there is one species using the available
resource in each ―niche-space‖ in the coexistence scheme (Figure 9).

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 How a Locality Can Have so Many Species? 193

Figure 8. Jaccard index of similarity (dashed line=75%) for the species sampled at the CIEM - Tinigua
National Park, Meta Department, Colombia.

All these mechanisms are the result of interactions between historical and ecological
factors (Davis & Scholtz 2001) and promote the coexistence of different species by limiting
the effect of the factors that are primarily responsible for high levels of interspecific
competition (Hanski 1980a, b, Giller & Doube 1989, Lumaret et al. 1992, Finn & Gittings
2003, Hutton & Giller 2004).

“Rare Species” and Sampling Recommendations

Over the course of the sampling process, some species appeared to be rare because of
their low abundances. However, when a new habitat or microhabitat was sampled, a new bait
or trap type was used, or sampling was conducted at a new time of the year, it was discovered
that that these ―rare‖ species were not rare at all, instead, their presence was underestimated
as a result of sampling inaccuracy. For example, this was the case for C. fulgidus, which
rarely occurred in ground-level pitfall traps but was common in 6 m elevation traps, for S.
faunus, which was collected when mist nets were used, and for S. leander, which was only
found on river beaches.
These examples of ―rare‖ species reveal how imprecise sampling can be and underscore
the necessity of using a sampling approach that includes a wide variety of trap types, a wide
range of bait types and sizes, and all possible habitats and microhabitats; that is carried out
over the entire year; and that incorporates more natural history studies.

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194 Jorge Ari Noriega A.

Figure 9. Coexistence scheme of the principal aspects of the niche segregation structure of the dung
beetles assemblage at the CIEM - Tinigua National Park, Meta Department, Colombia.

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 How a Locality Can Have so Many Species? 195

Finally, to more thoroughly characterize assemblage composition, exhaustive sampling

should take place over a full year and other kinds of traps should be used (Newton & Peck
1975, Moron & Terrón 1984, Noriega 2011). Furthermore, more specialized baits should be
utilized; these baits could include invertebrate feces, such as from earthworms (Matthews
1965, Howden & Young 1981), dead spirobolid millipedes (Bernon 1981, Cano 1998, Brühl
& Krell 2003), excrement from vertebrates found in the area (Martinez 1952, Young 1981a,
Janzen 1983, Gill 1991, Estrada et al. 1993), rotten fungi (Navarrete & Galindo 1997), and
other rare resources (Young 1980, Howden & Young 1981, Monteith & Storey 1981, Gill
1991, Villalobos et al. 1998, Pfrommer & Krell 2004).
In addition, it may be important to sample certain specific microhabitats, such as
bromeliads (Pereira et al. 1960, Huijbregts 1984, Cook 1998), caves (Zunino & Halffter
1988), mammal burrows (Zunino & Halffter 2007), ant nests (particularly made by the genera
Acromymex, Atta, Pheidole, and Solenopsis), and termite nests (Vaz-de-Mello et al. 1998,
Navarrete 2001). Lastly, the close (e.g., phoretic) relationships that some beetle species may
have with mammals such as sloths should not be forgotten (Ratcliffe 1980, Young 1981b).

ACKNOWLEDGMENTS
To the Japanese-Colombian cooperative agreement between the University of Los Andes
and the University of Myiagi. To the National Park Unit for granting the permits to carry out
research in Tinigua National Park. To Carlos Arturo Mejia, Ivan Jimenez, Daniel Cadena,
Alejandra Vega, Libia Carolina, Juan Cristobal Calle and Ramiro Montealegre for their help
in the field samplings. To Fernando Vaz-de-Mello, David Edmonds, Bruce Gill, Francois
Genier and Alejandro Lopera for their help in identifying the specimens. To Luis M.
Carrascal and Daniel Monroy for their important and valuable contributions and their help
with the statistical analyses in this paper. To Edison Torrado-Leon from Naturavision
(www.naturavision.com) for his significant support and collaboration in taking the photos of
the species. Ricardo Botero Trujillo made comments and suggestions that improved the
manuscript. To Pablo Stevenson for providing valuable information and references. To David
Morris and Jessica Pearce-Duvet for kindly checking the English version of the manuscript.

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