Anais da Academia Brasileira de Ciências (2013) 85(2): 679-697

(Annals of the Brazilian Academy of Sciences)

Printed version ISSN 0001-3765 / Online version ISSN 1678-2690
www.scielo.br/aabc

Diversity and seasonality of Scarabaeinae (Coleoptera: Scarabaeidae)

in forest fragments in Santa Maria, Rio Grande do Sul, Brazil

PEDRO G. DA SILVA1,3, FERNANDO Z. VAZ-DE-MELLO2 and ROCCO A. DI MARE3

1
Programa de Pós-Graduação em Ecologia, Departamento de Ecologia e Zoologia,
Universidade Federal de Santa Catarina, 88040-900 Florianópolis, SC, Brasil
2
Instituto de Biociências, Departamento de Biologia e Zoologia, Universidade Federal de Mato Grosso,
Avenida Fernando Corrêa da Costa, 2367, Boa Esperança, 78060-900 Cuiabá, MT, Brasil
3
Programa de Pós-Graduação em Biodiversidade Animal, Universidade Federal de Santa Maria,
Avenida Roraima, 1000, Camobi, 97105-900 Santa Maria, RS, Brasil

Manuscript received on April 13, 2012; accepted for publication on October 11, 2012

ABSTRACT
Scarabaeinae specimens were collected with the use of pitfall traps baited with human excrement, rotten
meat and rotting banana, between May 2009 and April 2010, in three forest fragments in Santa Maria,
Rio Grande do Sul, Brazil: ‘Morro do Elefante’ (MOEL), ‘Morro do Cerrito’ (MOCE) and ‘Campus da
Universidade Federal de Santa Maria’ (UFSM). A total of 19,699 individuals belonging to 33 species were
collected. Canthidium aff. trinodosum Boheman, 1858, Canthon latipes Blanchard, 1845, Dichotomius
assifer (Eschscholtz 1822), Eurysternus caribaeus (Herbst 1789), Canthidium sp. and Canthon lividus
Blanchard, 1845, were the most abundant species. MOEL showed the greatest richness, MOCE the greatest
abundance, while UFSM showed the lowest values of richness and abundance. The greatest similarity
(qualitative and quantitative) was found between MOEL and MOCE, while the lowest occurred between
MOCE and UFSM. Only 51% of the species were common to all three fragments. The richness and
abundance of Scarabaeinae were positively correlated with the air temperature. The richness of the fragment
decreased according to the smaller size and the greater degree of disturbance of vegetation structure.
Key words: Atlantic forest, dung beetles, Southern Brazil, species richness, temporal distribution.

INTRODUCTION most of the Brazilian biodiversity (Costa et al.

Human action has caused the reduction and loss 2000, Myers et al. 2000, Costa et al. 2005, Giulietti
of biodiversity (Favila and Halffter 1997, Medri et al. 2005, Mittermeier et al. 2005).
and Lopes 2001, Halffter 2005, Verdú et al. 2007) In Neotropical forests, the monitoring of
because of habitats transformation, fragmentation these alterations has been investigated by using
and loss, the so-called ‘erosion of biodiversity’ bioindicators (Brown-Jr. 1991, 1997, Halffter and
(Marques et al. 2002). In Brazil, this action is more Favila 1993, Favila and Halffter 1997, Brown-
evident in the alteration and the decline of its forests Jr. and Freitas 2000, Gardner et al. 2008). Among
(Fearnside 2005, Tabarelli et al. 2005), which retain these, Scarabaeinae (Coleoptera: Scarabaeidae) has
received special attention (Spector 2006) due to
Correspondence to: Pedro Giovâni da Silva
E-mail: [email protected] its strong relationship with the forest environment

An Acad Bras Cienc (2013) 85 (2)

680 PEDRO G. DA SILVA, FERNANDO Z. VAZ-DE-MELLO and ROCCO A. DI MARE

and mammals that live in these forests (Gill 1991, and Forsyth 2005, Gardner et al. 2008) and may
Halffter 1991) and because it has the necessary respond differently to these changes, altering their
characteristics for this purpose (Favila and Halffter abundance, richness and species composition.
1997, Spector 2006). Factors such as vegetation cover, vegetation
There are approximately 7,000 species of type, fragmentation, habitat loss, physical structure
Scarabaeinae worldwide (Schoolmeesters et al. and altitude of ecosystem, as well as human
2010), and the greatest diversity is concentrated in activity, influence the assembly of Scarabaeinae in
tropical forests and savannahs, forming a functionally different environments (Davis et al. 1999, Halffter
and taxonomically well-defined community (Halffter and Arellano 2002, Escobar et al. 2007). Thus,
and Edmonds 1982, Hanski and Cambefort 1991). many species are adapted to a particular type of
In Brazil, these beetles are known as ‘rola-bostas’ habitat or food resource (Davis 1996), and human
because they make, roll and bury small portions interference, which tends to alter the ecosystem,
of the ball-shaped food that serves as a substrate causes a major change in the assemblies, and may
to lay their eggs and as food to the larvae (Halffter influence on the rareness and local loss of species
and Matthews 1966, Hanski and Cambefort 1991, (Davis and Philips 2005).
Simmons and Ridsdill-Smith 2011). In Rio Grande do Sul there are two distinct
The dung beetles are detritivorous and biomes (Atlantic forest in the northern and the
promote the removal from and re-entry of organic Pampa in the southern) and they have suffered
matter in the soil where they feed themselves in great losses in area along decades because of the
the nutrients’ cycle (Halffter and Matthews 1966, transformation of their respective ecosystems
Hanski and Cambefort 1991). Hence, they help – forest and grassland (Bencke 2009, Instituto
clean the environment, and maintain and regulate Brasileiro de Geografia e Estatística, 2009,
the edaphic physical-chemical proprieties by Cordeiro and Hasenack 2009, Roesch et al. 2009).
burrowing, thus furnishing the soil with better Contrastingly, in many regions of Rio Grande do
aeration and hydration, as well as incorporating Sul the data about most of invertebrates are still
nutrients contained in dung, fruits and animal considered scarce (Bencke 2009, Roesch et al.
carcasses buried within the galleries (Halffter 2009), even though there are reports about the high
and Matthews 1966, Halffter and Edmonds 1982, number of endemic species that dependent of one
Hanski and Cambefort 1991, Nichols et al. 2008). or both biomes, and about the present conditions of
Currently, Scarabaeinae beetles have been degradation of these biomes (Bilenca and Miñarro
used in some countries (e.g. Australia, Brazil, 2004, Bencke 2009, Overbeck et al. 2009, Roesch
Chile and the USA) for the control of bovine et al. 2009, Inventário Florestal Contínuo 2010).
parasites (Waterhouse 1974, Bornemissza 1976, Despite of the fact that invertebrates are
Flechtmann and Rodrigues 1995, Koller et al. mostly constituted by the biodiversity of terrestrial
2007). The group has also been employed as an ecosystems, and are also important links in the
environmental indicator (Halffter and Favila trophic chain, the knowledge about Scarabaeinae
1993, Spector and Forsyth 1998, Davis et al. 1999, is scarce in Rio Grande do Sul, being Lepidoptera
2001, 2004, McGeoch et al. 2002, Spector 2006, and Hymenoptera the most in-depth species studied
Nichols et al. 2007, 2008), once these insects (Bencke 2009). Studies on beetles are still incipient
are very sensitive to changes in the ecosystem in Rio Grande do Sul (see Audino et al. 2007,
(Halffter and Favila 1993, McGeoch et al. 2002, Moura 2003, 2007), and within the order, only
Andresen 2003, Spector and Ayzama 2003, Larsen Cerambycidae and Chrysomelidae have been well

An Acad Bras Cienc (2013) 85 (2)

 DIVERSITY AND SEASONALITY OF DUNG BEETLES 681

investigated (Moura 2003). Recently, Scarabaeinae an area of ecological tension, and is an important
has been the focus of studies in extreme south environment that is a receptor of species from
Brazil (Silva et al. 2008, 2009, Audino et al. 2011, both biomes within Rio Grande do Sul.
Silva 2011), covering the ‘Campanha’ region of Rio In order to conduct the study, three different
Grande do Sul, within the Pampa biome. As well as non-contiguous forest habitats were chosen for
many regions of Brazil, the state still needs further the collection of Scarabaeinae beetles: a forest
surveying and the data on the species derive mostly with highly preserved vegetation, a forest with
from old-fashioned literature and taxonomic studies intermediate level of alteration and a forest with
of material in museums (Vaz-de-Mello 2000). intensive anthropogenic interference, with mass
Therefore, this study aims at determining plantation of exotic trees. The main criterion for
whether the Scarabaeinae assemblies are different choosing the areas was the degree of internal and
in forest fragments with different levels of surrounding disturbance (transformation) of the
disturbance in Santa Maria, Rio Grande do Sul, forest for diverse purposes.
Brazil. The temporal distribution of Scarabaeinae ‘Morro do Elefante’ (MOEL). Located near
was correlated with climate variables in order to the former primary school ‘Cidade dos Meninos’
find possible links between them. (29°40’33”S, 53°43’14”W), it is a non-isolated
remnant of the Seasonal Deciduous Forest of the
MATERIALS AND METHODS escarpment of ‘Planalto Médio Riograndense’ or
‘Fralda da Serra Geral’ (Machado and Longhi
STUDY AREA
1990). At the base of its southern face, there are
The municipality of Santa Maria is located in the small areas within the forest cultivated with Pinus
central portion of Rio Grande do Sul, with its sp., Eucalyptus sp. and Citrus sp., and the cutting
major part within the domain of the Pampa biome of trees in some properties, which are currently
and the northern part belonging to the Atlantic going through a process of regeneration. The total
Forest biome (Marchiori 2009, Instituto Brasileiro area of this forest fragment is around 729.3 ha
de Geografia e Estatística 2010). The climate in even though a major part is in an area of difficult
Santa Maria is subtropical rainy and warm, Cfa access, where the inclination is superior to 45°.
according to the classification of Köppen-Geiger The average altitude is 249 m (maximum of 465
(Pell et al. 2007) in which the average annual m) and within the forest there are some trails and
precipitation is 1,700 mm and the average annual clearings. The surrounding of the fragment is
air temperature is 19°C (Instituto Nacional de largely composed (at north and northwest) by a
Meteorologia 2010). Most of the municipality is chain of other hills with similar forest vegetation,
constituted of grassland lowlands and the forest and other areas with farms with livestock and
vegetation is restricted to watercourses and crops. It will be treated as forest area with a high
hillsides, the latter belonging to the Deciduous level of preservation.
Forest of the ‘Fralda da Serra Geral’ (Pereira et ‘Morro do Cerrito’ (MOCE). Located at ‘Centro
al. 1989). The municipality is in the transition Marista de Eventos’ (29°42’07”S, 53°47’08”W), it
zone between ‘Depressão Central’ and ‘Planalto is an isolated remnant of Deciduous Forest of ‘Serra
Meridional Brasileiro’, with altitudes ranging Geral’ and is part of ‘Depressão Central’ of Rio
from 40 to 500 m above sea level. According Grande do Sul (Pereira et al. 1989). Its approximate
to the Continuous Forest Inventory (Inventário area is 141.5 ha, the average elevation is 169 m,
Florestal Contínuo 2010), the city is located in with intermediate level of transformation of its

An Acad Bras Cienc (2013) 85 (2)

682 PEDRO G. DA SILVA, FERNANDO Z. VAZ-DE-MELLO and ROCCO A. DI MARE

forest vegetation into fields, and residences. The the insects fall (Lobo et al. 1988, Ausden 1996).
number of neighbor fragments normally composed A plastic bait-holder pot with smaller dimensions
by native vegetation is high, but the mean distance was put on a larger one in order to accommodate
among them is large, causing MOCE to become the baits. A solution of water, formalin (10%) and
increasingly isolated. It will be treated as forest detergent (neutral) was used inside the trap so as
area with intermediate level of preservation. to capture and preserve the specimens. A total of
‘Campus da Universidade Federal de Santa 27 traps were distributed along three transects over
Maria’ (UFSM). It is a forest area with high level of 100 m distant from each other in each one of the
disturbance (29°43’27”S, 53°43’29”W), currently fragments, and they were arranged in a triangle
constituted of a forest fragment with secondary shape of two meters of side, containing the three
native vegetation in the understory, the border and kinds of baits used. Each transect contained three
in smaller contiguous fragments, as well as mixed sets of three traps 30 m distant from each other. The
plantations of Pinus spp. and Eucalyptus spp. in the samplings were collected between May 1, 2009 and
surrounding (Dambros et al. 2004, Madruga et al. April 30, 2010, in fortnightly collections. Thus,
2007). The area size is approximately 35.2 ha, the there were two collections every month, the first at
average altitude is 95 m and there are buildings, the end of the first half, and the second at the end
grassland areas and crop areas in the surroundings. of the second half. The traps remained in the field
This fragment will be treated as forest area with during all time of duration of the study (for more
high level of disturbance. information, see Silva et al. 2012).
The distance between the fragments was The insects were captured and then transported
calculated by using the software Google Earth, in sealed plastic containers being properly labeled
there being 6.8 km between MOEL and MOCE, at the Laboratório de Biologia Evolutiva (LBEV)
6 km between MOCE and UFSM, and 4.8 km at Universidade Federal de Santa Maria, where
between MOEL and UFSM (for more information, they were sorted, counted, pre-identified and
see Silva et al. 2012). accommodated in entomological blankets and
boxes, and in bottles with alcohol 70%. The pre-
SAMPLING METHOD identification was carried out through the use of a
key to genera of Scarabaeinae (Vaz-de-Mello et al.
The specimens were collected through the use of 2011) and their comparison with specimens that had
baited pitfall traps, once they correspond to the most already been deposited at the laboratory; and they
efficient sampling method for the capture of most were separated into morphospecies when unknown.
of this group (Lobo et al. 1988, Halffter and Favila Individuals of all species and morphospecies were
1993, Favila and Halffter 1997, Spector 2006). then identified by the second author. The material is
The traps were baited with human feces, chicken currently in the collections of Universidade Federal
offal (heart) and banana (the two latter were rotten de Santa Maria, Santa Maria, RS and Universidade
in plastic pots at ambient temperature for three Federal de Mato Grosso, Cuiabá, MT.
days), corresponding to the insects’ main diets:
coprophagy, necrophagy and saprophagy (Halffter DATA ANALYSIS
and Matthews 1966, Hanski and Cambefort 1991).
The traps consisted of a one-liter plastic The assembly of Scarabaeinae was described
container with 13 cm diameter and 10 cm height, in relation to richness (S or alpha diversity),
buried with the edge kept at soil level to allow abundance (N), species composition, similarity

An Acad Bras Cienc (2013) 85 (2)

 DIVERSITY AND SEASONALITY OF DUNG BEETLES 683

among fragments, species spatial exchange presented by Silveira-Neto et al. (1976), being the
among habitats (beta diversity) and equitability species classified as: constant (those present in more
(Moreno 2001). The distribution of abundance than 50% of samples), accessory (present in 25-
among species of Scarabaeinae was graphically 50%) and accidental (present in less than 25%).
compared among the fragments through ranks, The diversity of each habitat sampled was
where the relative abundance of each species calculated through the indexes of Shannon-Wiener
was transformed into a logarithm of base 10 (N (H’) and Margalef (DMg) (Moreno 2001). The
+ 1) and arranged from highest to lowest value dominance indexes of Simpson (D) and Berger-
for each habitat (Verdú et al. 2007). Parker (d) were calculated in order to assess the level
From the number of species and individuals of dominance in the assemblies of Scarabaeinae
obtained in each collection smoothed curves of (Magurran 1988, Moreno 2001). All these indexes
sample sufficiency were made for each of the were estimated through the software PAST 2.02.
fragments (Mao Tau function of EstimateS software In order to verify the qualitative similarity
[Colwell 2004]) in order to verify the sample among the habitats, the coefficients of Jaccard
sufficiency. The estimated richness was obtained (IJ) and Sorensen (IS) were used. The index of
through the estimators Chao 1, Chao 2, Jackknife Morisita-Horn (IMH) and the quantitative coefficient
1, Jackknife 2, and Bootstrap (and their confidence of Sorensen (ISquant) were calculated to verify the
intervals at 95%). The software EstimateS 7.0 was quantitative similarity among the fragments (Moreno
used for both analyses (Colwell 2004) with 500 2001). Based on the similarity values obtained, the
replacement randomizations for the analysis of the beta diversity was calculated through qualitative and
estimators and no randomization for the construction quantitative data, thus subtracting 1 (one) from the
of the accumulation curves (Colwell 2004). similarity value (Verdú et al. 2007).
The rarefaction method (Hulbert 1971) was The equitability was calculated with the Pielou
conducted with the software PAST 2.02 Hammer index (J’) (Magurran 1988). The data normality
& Harper, Norway (Hammer et al. 2001). The was assessed through the Shapiro-Wilk test with
abundance of the fragments was compared with the software PAST 2.02.
the software PAST 2.02 through an ANOVA test, in
METEOROLOGICAL DATA
which the total abundance values of each transect
were used. The data of air temperature (minimum, average and
The species behavioral guild was attributed maximum), pluvial precipitation, relative humidity
according to literature (Halffter and Edmonds and insolation period between May 2009 and
1982, Cambefort and Hanski 1991, Doube 1991, April 2010 were provided by the Meteorological
Gill 1991), being the species classified as tunnelers Station at Universidade Federal de Santa Maria
(take food from and carry it to galleries constructed (Departamento de Fitotecnia), linked to the
beneath or next to the food source), rollers (rotate Instituto Nacional de Meteorologia (INMET). The
portions of food to bury them in distant galleries) INMET basis for data collection covers a radius of
or dwellers (remain in the food source, feeding 20 km and the areas studied are within this range
themselves and nesting there). allowing the test of correlation to be realized.
The group of dominant species was qualified The monthly number of species and indi-
as the sum of their relative abundance reached a viduals of Scarabaeinae was correlated with
minimum of 70%. The constancy of species along the meteorological data through the coefficient of
period of collection was calculated using the formula Pearson (RP) in order to find possible relationships

An Acad Bras Cienc (2013) 85 (2)

684 PEDRO G. DA SILVA, FERNANDO Z. VAZ-DE-MELLO and ROCCO A. DI MARE

between the abiotic variables and the temporal RESULTS

distribution of species. In order to homogenize the The collections resulted in a total of 19,699
variance, the data were transformed on the square individuals, belonging to six tribes, 13 genera and
root of their initial values. A discussion about the 33 species. Among the three habitats sampled,
number of individuals and species per month of Canthidium aff. trinodosum Boheman, 1858
collection and season is presented. (24.9%), Canthon latipes Blanchard, 1845 (1.4%),

TABLE I
Species of Scarabaeinae (Coleoptera: Scarabaeidae) sampled using baited pitfall traps in three forest fragments
in Santa Maria, Rio Grande do Sul, Brazil, between May 2009 and April 2010. MOEL: ‘Morro do Elefante’;
MOCE: ‘Morro do Cerrito’; UFSM: ‘Campus da Universidade Federal de Santa Maria’. (*) indicate species
found only in one habitat. S: number of species; N: number of individuals; %: percentage of individuals in
relation to the total captured; BG: behavioral guild; D: dweller; R: roller; T: tunneler; CO: constancy; A:
constant; B: accessory; C: accidental. The number of each species is used to differentiate them in Figure 1.

Habitats
Tribe/species Total % BG CO
MOEL MOCE UFSM
Ateuchini (S = 3; N = 195)
1. Ateuchus aff. carbonarius (Harold, 1868) * 0 1 0 1 0.01 T C
2. Ateuchus aff. robustus (Harold, 1868) 13 24 31 68 0.35 T B
3. Uroxys aff. terminalis Waterhouse, 1891 19 100 7 126 0.64 T A
Coprini (S = 10; N = 10,221)
4. Canthidium aff. dispar Harold, 1867 257 210 1 468 2.38 T A
5. Canthidium moestum Harold, 1867 33 2 17 52 0.26 T B
6. Canthidium aff. trinodosum (Boheman, 1858) 3,048 1,854 21 4,923 24.9 T A
7. Canthidium sp. 592 450 4 1,046 5.31 T A
8. Dichotomius aff. acuticornis (Luederwaldt, 1930) 9 17 0 26 0.13 T B
9. Dichotomius assifer (Eschscholtz, 1822) 346 2,659 0 3,005 15.2 T A
10. Dichotomius nisus (Olivier, 1789) 4 2 22 28 0.14 T B
11. Homocopris sp. * 2 0 0 2 0.01 T C
12. Ontherus azteca Harold, 1869 15 22 6 43 0.22 T B
13. Ontherus sulcator (Fabricius, 1775) 75 188 365 628 3.19 T A
Deltochilini (S = 11; N = 6,216)
14. Canthon amabilis Balthasar, 1939 34 215 0 249 1.26 R B
15. Canthon chalybaeus Blanchard, 1845 27 7 399 433 2.2 R A
16. Canthon latipes Blanchard, 1845 739 2,492 0 3,231 16.4 R A
17. Canthon lividus Blanchard, 1845 563 118 5 686 3.48 R A
18. Canthon aff. luctuosus Harold, 1868 195 305 2 502 2.55 R A
19. Canthon oliverioi Pereira & Martínez, 1956 58 22 0 80 0.41 R B
20. Canthon quinquemaculatus Castelnau, 1840 17 2 447 466 2.37 R A
21. Deltochilum brasiliense (Castelnau, 1840) 16 8 0 24 0.12 R B
22. Deltochilum morbillosum Burmeister, 1848 26 5 0 31 0.16 R B
23. Deltochilum rubripenne (Gory, 1831) 135 359 3 497 2.52 R A
24. Deltochilum sculpturatum Felsche, 1907 5 0 12 17 0.09 R B

An Acad Bras Cienc (2013) 85 (2)

 DIVERSITY AND SEASONALITY OF DUNG BEETLES 685

TABLE I (CONTINUATION)

Habitats
Tribe/species Total % BG CO
MOEL MOCE UFSM
Phanaeini (S = 4; N = 627)
25. Coprophanaeus milon (Blanchard, 1845) 2 0 39 41 0.21 T B
26. Coprophanaeus saphirinus (Sturm, 1826) 277 280 0 557 2.83 T A
27. Phanaeus splendidulus (Fabricius, 1781) 14 11 0 25 0.13 T C
28. Sulcophanaeus rhadamanthus (Harold, 1875) * 4 0 0 4 0.02 T C
Oniticellini (S = 3; N = 1,576)
29. Eurysternus aeneus Génier, 2009 * 0 0 1 1 0.01 D C
30. Eurysternus caribaeus (Herbst, 1789) 407 962 73 1,442 7.32 D A
31. Eurysternus parallelus Castelnau, 1840 47 83 3 133 0.68 D A
Onthophagini (S = 2; N = 864)
32. Onthophagus catharinensis Paulian, 1936 55 453 0 508 2.58 T A
33. Onthophagus aff. tristis Harold, 1873 53 238 65 356 1.81 T A
Number of individuals 7,087 11,089 1,523 19,699
Number of species 31 28 20 33

Dichotomius assifer (Eschscholtz 1822) (15.2%), species and together accounted for 72.7% of the
Eurysternus caribaeus (Herbst 1789) (7.3%), total number of individuals captured (Table I).
Canthidium sp. (5.3%) and Canthon lividus The composition of dominant species among the
Blanchard, 1845 (3.4%) were the most abundant investigated fragments was different (Figure 1). The
five dominant species (15.1%) in MOEL were C. aff.
trinodosum (43%), C. latipes (10.4%), Canthidium
sp. (8.3%), C. lividus (7.9%) and E. caribaeus (5.7%),
that together totaled 75.4% of the total number of
individuals. In MOCE, the four species (14.2%)
that together represented 71.8% of the total were D.
assifer (23.9%), C. latipes (22.4%), C. aff. trinodosum
(16.7%) and E. caribaeus (8.6%). The fragment
UFSM showed 79.5% of dominance of three species
(15%): Canthon quinquemaculatus (Castelnau 1840)
(29.3%), C. chalybaeus Blanchard, 1845 (26.2%) and
Figure 1 - Rank-abundance plots (N) of Scarabaeinae species Ontherus sulcator (Fabricius 1775) (23.9%).
(Coleoptera: Scarabaeidae) captured by pitfall traps baited
All the sampling sufficiency curves reached
with human excrement, rotten meat and rotten bananas in
three forest fragments in Santa Maria, Rio Grande do Sul, an asymptote (Figure 2), demonstrating how
Brazil, between May 2009 and April 2010. MOEL: ‘Morro successful was the capture of the species of
do Elefante’; MOCE: ‘Morro do Cerrito’; UFSM: ‘Campus da Scarabaeinae attracted by the baits used in the three
Universidade Federal de Santa Maria’. The relative abundance
habitats sampled.
of each species was transformed into logarithm base 10
(N + 1) and arranged from highest to lowest value for each The number of species detected in each
habitat. The numbers are relative to species in Table I. fragment was approximate to the expected, based

An Acad Bras Cienc (2013) 85 (2)

686 PEDRO G. DA SILVA, FERNANDO Z. VAZ-DE-MELLO and ROCCO A. DI MARE

on the richness estimators (Chao 1 and 2, Jackknife

1 and 2, and Bootstrap) (Table II) and they indicated
the efficiency in the sampling of the local richness.
To MOEL, the minimum capture was approximately
98.6% of the estimated Scarabaeinae fauna. In
MOCE it was 91.7%, and in UFSM 97%.
In order to standardize the abundance in 1,523
individuals for each fragment, the method of rare-
faction was used and it was possible to evidence

TABLE II
Observed and estimated (with standard deviation)
richness of Scarabaeinae (Coleoptera: Scarabaeidae) for
the forest fragments sampled with baited pitfall traps
in Santa Maria, Rio Grande do Sul, Brazil, between
May 2009 and April 2010. MOEL: ‘Morro do Elefante’;
MOCE: ‘Morro do Cerrito’; UFSM: ‘Campus da
Universidade Federal de Santa Maria’.

Habitats
Estimators
MOEL MOCE UFSM
Observed
31 28 20
richness
Bootstrap 31.25 ± 0.62 28.29 ± 1.74 20.32 ± 0.85
Chao 1 30.91 ± 0.18 27.59 ± 0.36 20.08 ± 0.56
Chao 2 31.28 ± 0.74 30.51 ± 2.79 20.38 ± 1.21
Jackknife 1 31.43 ± 0.61 29.99 ± 1.49 20.60 ± 0.83
Jackknife 2 31.01 ± 1.91 28.91 ± 4.95 19.88 ± 2.47

Figure 2 - Sample sufficiency curve (Mao Tau function) for Figure 3 - Rarefaction curve with standard deviation for the
three forest fragments sampled with baited pitfall traps in assemblies of Scarabaeinae (Coleoptera: Scarabaeidae) captured
Santa Maria, Rio Grande do Sul, Brazil, between May 2009 using baited pitfall traps in three forest fragments in Santa Maria,
and April 2010. MOEL: ‘Morro do Elefante’; MOCE: ‘Morro Rio Grande do Sul, Brazil, between May 2009 and April 2010.
do Cerrito’; UFSM: ‘Campus da Universidade Federal de MOEL: ‘Morro do Elefante’; MOCE: ‘Morro do Cerrito’;
Santa Maria’. UFSM: ‘Campus da Universidade Federal de Santa Maria’.

An Acad Bras Cienc (2013) 85 (2)

 DIVERSITY AND SEASONALITY OF DUNG BEETLES 687

that the assemblies of Scarabaeinae were similar to number of individuals per transect, since these are
what had been previously observed, with greater larger and more preserved fragments than UFSM.
richness in the largest and most preserved fragment The greatest value of the dominance index of
MOEL (S = 28.4 ± 1.18), intermediate richness in Berger-Parker occurred in MOEL (d: 0.430) (Table
MOCE (S = 23.3 ± 1.30) and lowest richness in the III), and expressed the greatest proportion of the
smallest and most disturbed fragment (20) (Figure 3). most abundant species (C. aff. trinodosum – 43%)
There was a significant statistical difference in in this fragment in relation to the total number of
the distribution of the abundance of Scarabaeinae individuals, differently from what occurred in
in the fragments (F = 14.875; d.f. = 2; p < 0.01), the other two habitats. The Simpson index also
where only MOEL and MOCE did not differ in showed a higher value for MOEL (D: 0.219).
TABLE III
Measures’ summary of richness, abundance, diversity, evenness and similarity of Scarabaeinae (Coleoptera:
Scarabaeidae) in each forest fragment sampled in Santa Maria, Rio Grande do Sul, Brazil. MOEL: ‘Morro do Elefante’;
MOCE: ‘Morro do Cerrito’; UFSM: ‘Campus da Universidade Federal de Santa Maria’.

Habitats
Parameter evaluated Total
MOEL MOCE UFSM
Total abundance 7,087 11,089 1,523 19,699
Monthly mean abundance 295,29 462,04 63,46 820,79
Abundance in pitfalls with meat 2,094 193 705 3,992
Abundance in pitfalls with feces 4,529 9,500 745 14,774
Abundance in pitfalls with bananas 464 396 73 933
Total richness 31 28 20 33
Estimated richness 31.18 28.86 20.25 33.26
Monthly mean richness 12.87 12.87 5.50 17.87
Richness in pitfalls with meat 28 22 15 29
Richness in pitfalls with feces 31 27 18 33
Richness in pitfalls with bananas 21 19 10 25
Tunnelers 18 16 11 19
Dwellers 2 2 3 3
Rollers 11 10 6 11
Singletons 0 1 2 2
Doubletons 2 3 1 1
Restricted species 2 1 1 -
Shared species 29 27 19 -
Pielou’s evenness 0.622 0.677 0.614 0.709
Margalef index 3.384 2.899 2.593 3.236
Shannon-Wiener index 2.135 2.257 1.839 2.479
Berger-Parker index (dominance) 0.430 0.239 0.293 0.249
Simpson index (dominance) 0.219 0.151 0.218 0.128
Jaccard mean qualitative similarity1 0.719 0.696 0.571 -
1
Sorensen mean qualitative similarity 0.830 0.812 0.727 -
Morisita-Horn mean quantitative similarity1 0.356 0.357 0.064 -
1
Sorensen mean quantitative similarity 0.321 0.314 0.073 -
1
Mean between habitats.

An Acad Bras Cienc (2013) 85 (2)

688 PEDRO G. DA SILVA, FERNANDO Z. VAZ-DE-MELLO and ROCCO A. DI MARE

This index, strongly influenced by the set of the 1868) (singleton) was evidenced only in MOCE;
most abundant species (Magurran 1988), showed and Eurysternus aeneus Génier, 2009 (singleton)
higher values for these fragments due to the greater occurred only in UFSM.
proportion of dominant species, accounting for The data concerning observed and rarefied
more than 75% of individuals in these habitats, the richness indicated higher alpha diversity (31 species)
same not occurring in MOCE. for the largest and most preserved area (MOEL) in
MOEL showed a lower equitability value than relation to the other two fragments. MOCE held the
MOCE (Table III), though it clearly presented highest value for the diversity index of Shannon-
more richness and smaller number of individuals. Wiener (2.257), influenced by the greatest equitability
The influence of the greatest number of species (0.681) showed in this fragment. However, no
represented by few individuals present in MOEL significant difference was found between MOCE
may have contributed to these results, and also to and MOEL. The Margalef index was the highest for
the values of dominance found in this fragment. MOEL (3.384), since it showed the highest richness
In total, 17 species (51.5%) were classified with less total abundance than MOCE, there being
as constants, from which four showed constancy significant difference among all three fragments.
above 90%, five between 75-90% and eight The qualitative similarity for the three fragments
between 50-75%. Eleven species (33.4%) were calculated through the coefficients of Jaccard and
classified as accessory, being five (15.1%) Sorensen showed higher values between MOEL
accidental, three of which classified as uniques and MOCE (Table IV), since the number of species
(occurred in one sample only) and one duplicate shared between the two habitats (27) was elevated.
(occurred in two samples only). In MOEL, 11 When paired with UFSM the two fragments showed
species (35.5%) were constants, and only one similarity lower than 60% according to Jaccard,
showed higher constancy than 90% (C. aff. and lower than 75% according to Sorensen, a result
trinodosum). Twelve species (38.7%) were which was strongly influenced by the difference in the
accessory and eight (25.8%) accidental (one unique richness of each fragment. The quantitative similarity
and two duplicates). In MOCE, 14 species (50%) expressed by the indexes of Morisita-Horn and
were classified as constants, two of which showed Sorensen (quantitative) was also higher for areas with
constancy above 90% (C. aff. trinodosum and D. the highest percentage of natural forest vegetation
assifer). Five species (17.8%) were accessory, (MOEL and MOCE) and, when paired with UFSM,
while nine (32.2%) were accidental (five uniques they showed very low similarity indexes due to the
and one duplicate). In UFSM, only four species great differences in richness, abundance and species
(20%) were constants, and no one showed more dominance among the pairs of fragments.
than 75% of constancy. Five species (25%) were The qualitative beta diversity, or the degree
accessory and eleven (55%) were classified as of rearrangement of species, was more evident
accidental (two uniques and three duplicates). between MOCE and UFSM due to the smaller
Considering the three habitats, 19 species (57.5%) number of shared species (17) between these
were tunnelers, 11 (33.4%) rollers and only three fragments. When using quantitative data, the
(9.1%) were dwellers. degree of difference becomes 93.7% between the
The species restricted to only one fragment were most preserved and the most disturbed habitats.
Homocopris sp. (doubleton) and Sulcophanaeus The greatest abundance of Scarabaeinae
rhadamanthus (Harold 1875), which occurred between the months of collections was found in
only in MOEL; Ateuchus aff. carbonarius (Harold October (4,759 individuals – 24.2%), November

An Acad Bras Cienc (2013) 85 (2)

 DIVERSITY AND SEASONALITY OF DUNG BEETLES 689

TABLE IV
Qualitative and quantitative similarity values of Scarabaeinae (Coleoptera: Scarabaeidae) fauna between pair of forest
fragments sampled in Santa Maria, Rio Grande do Sul, Brazil, between May 2009 and April 2010. In parenthesis, beside the
values of similarity is given the values of beta diversity calculated by deducting the value of similarity of 1 (one) (Verdú et al.
2007). MOEL: ‘Morro do Elefante’; MOCE: ‘Morro do Cerrito’; UFSM: ‘Campus da Universidade Federal de Santa Maria’.

Pairs of forest fragments

Indexes
MOEL x MOCE MOEL x UFSM MOCE x UFSM
Jaccard (IJ) 0.844 (0.156) 0.594 (0.406) 0.548 (0.452)
Sorensen - qualitative (IS) 0.915 (0.085) 0.745 (0.255) 0.708 (0.292)
Morisita - Horn (IMH) 0.649 (0.351) 0.063 (0.937) 0.065 (0.935)
Sorensen - quantitative (ISquant) 0.562 (0.438) 0.079 (0.921) 0.066 (0.934)

(4,162 individuals – 21.1%) and December (3,336 January: 26 species each), as well as the smallest
individuals – 16.9%), representing 62.2% of the richness captured (July: eight species). The Pearson
total individuals captured (Figure 4a). The other correlation test found a positive relation between
months remained under 2,000 individuals per richness and abundance variables (RP = 0.83; p <
collection. July 2009 was the month with the lowest 0.0001). For each fragment, November was the
abundance (118 individuals – 0.6%). month with the greatest abundance and richness
The greatest richness also coincided with for MOEL (N = 1,487; S = 28) and UFSM (N =
the period of greatest abundance (October: 30 571; S = 14), while October with the highest values
species; November: 29 species; December and for MOCE in terms of species (26) and individuals
(3,154). In general terms, July and June respectively
were the months of lowest richness and abundance
among the fragments, coinciding with the period of
the lowest temperatures in the region.
Among the seasons, spring was the one with the
greatest abundance and richness (11,923 individuals

TABLE V
Pearson’ linear correlation between environmental
variables and abundance and richness of Scarabaeinae
(Coleoptera: Scarabaeidae) collected using baited pitfall
traps in three forest fragments in Santa Maria, Rio
Grande do Sul, Brazil, between May 2009 and April
2010. Asterisks indicate statistical significance at level of
0.05 (*) and 0.01 (**) probability.

Environmental variables Abundance Richness

Relative humidity (%) -0.26 -0.38
Minimum temperature (°C) 0.44* 0.72**
Figure 4 - Number of individuals and species of Scarabaeinae Mean temperature (°C) 0.43* 0.72**
(Coleoptera: Scarabaeidae) collected per month in Santa Maximum temperature (°C) 0.41* 0.70**
Maria, Rio Grande do Sul, Brazil, between May 2009 and
Precipitation (mm) 0.31 0.29
April 2010 (A) and distribution of environmental variables
during the study period (B). Insolation (h) 0.13 0.26

An Acad Bras Cienc (2013) 85 (2)

690 PEDRO G. DA SILVA, FERNANDO Z. VAZ-DE-MELLO and ROCCO A. DI MARE

– 31 species), followed by summer (4,010 individuals Louzada and Silva 2009, Silva et al. 2009, Lopes et
– 29 species). Autumn had the lowest abundance al. 2011, Silva 2011), as well as other Neotropical
(1,798), and winter the smallest richness (24). Similar countries such as Bolivia (Spector and Ayzama
patterns were found for each area, in which spring 2003), Colombia (Martínez et al. 2009), Ecuador
had the greatest abundance, followed by summer. (Peck and Forsyth 1982), Mexico (Halffter et al.
In relation to richness, spring presented the highest 1992) and Uruguay (Morelli et al. 2002).
number of species collected, followed by summer, By using the method of rarefaction it
except for the most disturbed area (UFSM), where was possible to observe that the assemblies of
the second highest number of species (richness) was Scarabaeinae appeared in a similar manner to
found in autumn and not in summer. what had been observed. The characteristics of
Among the climatic variables evaluated the interior and the surroundings of the fragments
(Figure 4b), air temperature was the only variable appear to have contributed to the results. Another
positively correlated with abundance and richness important factor is the availability of food (Halffter
of Scarabaeinae during the period of collection and Matthews 1966), since mammals are more
(Table V). likely to settle and remain in larger and more
preserved ecosystems. Thus, they contribute to the
DISCUSSION increase in the availability of dung and carcasses
for the fauna of Scarabaeinae. It is likely that
The richness of Scarabaeinae (33) does not differ environments closer to natural might harbor species
much from that found in other studies which made of fruit trees, provide a greater supply of food
use of baited pitfall traps in forest fragments in resources to generalist species of Scarabaeinae.
South and Southeastern Brazil (Lopes et al. 1994, A greater number of tunnellers in relation to
Louzada and Lopes 1997, Medri and Lopes 2001, other behavioral guilds was found. This pattern
Almeida and Louzada 2009, Hernández and in which there is a larger number of tunnellers is
Vaz-de-Mello 2009). According to the curves of common in Neotropical forests (Halffter et al. 1992,
sample sufficiency and the richness estimators, Louzada and Lopes 1997) and was also detected
the capture of the Scarabaeinae in the sampled in each of the fragments sampled. Apparently, the
fragments was satisfactory. constant proportional distribution in behavioral
The number of dominant species increased guilds seems to be the result of local diversity
according to the size and the decrease in the level of tribes of Scarabaeinae in Neotropical forests
of fragment’s alteration. According to Halffter (Louzada and Lopes 1997). On the other hand, the
(1991), Scarabaeinae is represented by a few proportion of tribes, genera and species captured
abundant species and many species with few with baits is restricted to a greater part of the
individuals in Neotropical forests. This pattern has Scarabaeinae fauna, since several groups of species
been often found in studies conducted in forest are generally not attracted by baited traps (see Vaz-
ecosystems (e.g., Louzada and Lopes 1997, Vaz- de-Mello et al. 1998, Vaz-de-Mello 2007, Vaz-
de-Mello 1999, Medri and Lopes 2001, Milhomem de-Mello and Génier 2009). Thus, the interaction
et al. 2003, Endres et al. 2007, Louzada et al. 2007, among the diversity of groups in the neotropics and
Filgueiras et al. 2009, Hernández and Vaz-de-Mello the use of baits compatible with the feeding habits
2009, Audino et al. 2011, Lopes et al. 2011, Silva of most species seems to reflect the pattern found.
2011), in areas of fields or pastures in Brazil (e.g., Even though represented by few individuals,
Koller et al. 2007, Matavelli and Louzada 2008, the species restricted to only one fragment are

An Acad Bras Cienc (2013) 85 (2)

 DIVERSITY AND SEASONALITY OF DUNG BEETLES 691

important for understanding the differences found 2002). Some Neotropical species of Scarabaeinae
in them. Homocopris sp. and S. rhadamanthus were show high habitat specificity (Halffter 1991),
restricted to MOEL, Ateuchus aff. carbonarius was especially for forest ecosystems, and thus, cannot
registered only in MOCE, and E. aeneus occurred extend their populations to open areas (Klein 1989,
only in UFSM. In Brazil, Homocopris Burmeister, Spector and Ayzama 2003, Almeida and Louzada
1846, contains species restricted to the remnants of 2009). Such species are strongly influenced by
the Atlantic Forest, located throughout southeast habitat loss and fragmentation, which may have
and south of the country, currently under review their distribution restricted or even disappear
where the species captured is being described (Vaz- locally (Davis and Philips 2005).
de-Mello et al. 2010). Sulcophanaeus Olsoufieff, The occurrence of species common to MOEL
1924 was reviewed by Edmonds (2000) and and UFSM may better illustrate the previously
Arnaud (2002), comprising coprophagous or described situation, because the influence of open
copro-necrophagous species and some, such as areas in these fragments is much higher than in
S. rhadamanthus, a rare species of Scarabaeinae MOCE. The similarity in species composition
with an unknown biology, but apparently related between MOEL and MOCE may be the result of
to fungi or mammal’s burrows (Edmonds 2000). previous processes being the latter apparently
Eurysternus Dalman, 1824 was reviewed by linked to the large set of hills with Deciduous Forest
Génier (2009), which stated that E. aeneus occurs vegetation that occurs in the north side of Santa
in forested areas across southern Brazil, southern Maria, and that has become increasingly isolated
Paraguay and northeast Argentina. Its occurrence along the years due to human expansion around this
in exotic forest ecosystems is also known (authors’ location. The fragment of UFSM, being situated on
personal observation). a flat terrain may have suffered a previous process of
The influence of the high level of alteration, the occupation, where the forest vegetation constituted
isolation, the ‘rural’ surroundings and the smallest primarily by gallery forest expanded along water
size may greatly contribute to the elevated rate of courses, was removed and gave way to fields,
beta diversity among the most disturbed fragment pastures and crops. Thus, the current Scarabaeinae
and the ones which show more well preserved fauna remaining in the fragment seems to be mostly
natural forest vegetation. Halffter and Arellano species originally occurring in open areas, and
(2002) assume that differences among habitats the size of this fragment, partly transformed into
found in their study (Veracruz, Mexico) and also in monocultures, is not sufficient to harbor most of the
other locations brought into discussion, are due to typically forest species.
vegetation cover and landscape heterogeneity, not Therefore, conservationist measures should
solely because of food availability. The landscape consider as both forest and grassland are important
heterogeneity can contribute to the survival of ecosystems for the communities of Scarabaeinae,
species that occur only in forested or in open because both are complementary and may show
areas (Halffter and Arellano 2002). In this sense, a particularly unique diversity that increases
the reduction in area of forested fragments, by the the diversity of the landscape (Almeida and
expansion of pastures and/or agricultural areas, or Louzada 2009). Although environments such as
even their transformation into forest cultures, can monocultures of exotic trees, very common in
affect the survival of species that occur in forests Brazil, may contribute to the beta diversity, they
and promote the expansion of species that prefer are not an ecosystem suitable for the maintenance
or adapt better in open areas (Halffter and Arellano of Scarabaeinae (Gardner et al. 2008).

An Acad Bras Cienc (2013) 85 (2)

692 PEDRO G. DA SILVA, FERNANDO Z. VAZ-DE-MELLO and ROCCO A. DI MARE

Differently from what occurs in tropical a greater number of Scarabaeinae species during
forests where rainfall affects the seasonality of the summer in Semi-Deciduous Secondary forest in
Scarabaeinae fauna (Halffter and Matthews 1966, Viçosa, Minas Gerais, Brazil, possibly influenced
Andresen 2008), the temperature is apparently the by temperature and precipitation.
main cause for the seasonality of Scarabaeinae Hernández and Vaz-de-Mello (2009) found a
in subtropical forests and even other types of relationship between Scarabaeinae abundance and
ecosystems in the subtropical regions. Halffter and richness and warm and rainy period in Mesophytic
Matthews (1966) stated that in temperate regions, Semi-Deciduous forest in São Paulo, Brazil,
adult specimens of Scarabaeinae usually nest in late establishing a strong correlation between the number
spring and early summer. Then, as soon as new adults of species and the average temperature. These authors
hatch (in the middle or late summer), they go through also observed a relationship between temperature
a hibernation period, which ends at the beginning and precipitation, both of which likely to influence
of the following spring, spending the winter in the distribution of Scarabaeinae in that location.
their nests in the soil (Halffter and Matthews 1966). Hernández (2007) found a correlation between the
Thus, the expressive richness and abundance of number of species and individuals of Scarabaeinae
Scarabaeinae found here in spring and summer and the rates of precipitation in Paraíba, Brazil.
follow the pattern described above. However, there However, the climate in this region is semi-arid, the
was capture along the entire period of study, even temperature undergoes little variation throughout
though in winter and autumn the numbers were the year, and the rainy season is the main factor that
very low. Normally, the collected species were those influences the dynamics of Scarabaeinae in these
that showed high abundance and were among the regions (Andresen 2008). For Scarabaeidae ((sensu
dominants of each fragment. Due to the large number lato) attracted by light traps in Santa Maria, RS, D.
of individuals, it is likely that these species reproduce Link (unpublished data) found a positive correlation
and nest in late summer and early autumn, and emerge between the distribution of this fauna and variables of
in shorts periods of mild temperatures during winter, nebulosity and insolation; and a negative correlation
once microclimatic effects within the fragment can between evaporation and wind speed. While studying
contribute to this fact (Hernández and Vaz-de-Mello the Scarabaeoidea fauna of this region, this author
2009). In general, the most uncommon species concluded that Scarabaeidae ((sensu lato) has no
are more easily captured in the period of elevated activity in temperatures below 7°C, and above 37.4°C
temperatures, while the most abundant species occur there is generally no activity of Scarabaeoidea.
throughout the year (Louzada and Lopes 1997). Thus, due to the climatic conditions the region
The relationship between greater abundance features, the temperature seems to be the main or
and greater richness for periods of high temperatures most evident climatic factor that affects the activity
is well known, especially for temperate regions, of Scarabaeinae in subtropical climates, although
where the insect species show a decrease in activity its relationship with other factors not assessed here
in low temperatures and increase in periods of could influence the dynamics of this fauna (Halffter
higher temperatures (Wolda 1988, Begon et al. and Matthews 1966, D. Link, unpublished data).
2007). Morelli et al. (2002) confirmed this pattern Very low temperatures, such as the ones occurring in
to the assemblies of Scarabaeinae in Uruguayan the region in certain periods of the year, tend to cause
prairies, where the average temperature of air and death or hibernation of the specimens, which may,
soil was determinant for the species abundance and in most cases, go through this period of unfavorable
richness. Louzada and Lopes (1997) also reported climate in larval form (Halffter and Matthews 1966).

An Acad Bras Cienc (2013) 85 (2)

 DIVERSITY AND SEASONALITY OF DUNG BEETLES 693

Microclimatic factors, structure of the area and the scholarship. This work has been partially supported
soil, inter and intraspecific competition may also by FAPEMAT (570847/2008 and 447441/2009)
affect the structure, composition, diversity and and CNPq (151603/2007-3 and 304925/2010-1).
abundance of Scarabaeinae in different ecosystems
RESUMO
(Halffter and Matthews 1966, Davis et al. 1999,
Halffter and Arellano 2002, Escobar et al. 2007, Espécimes de Scarabaeinae foram coletados com o
Nichols et al. 2007, Gardner et al. 2008), and they uso de armadilhas de queda iscadas com excremento
need further assessment. humano, carne apodrecida e banana em decomposição,
The great richness evidenced in Santa Maria, entre maio de 2009 e abril de 2010, em três fragmentos
including rare species of Scarabaeinae, adds florestais em Santa Maria, Rio Grande do Sul, Brasil:
important data to the fauna records of the central Morro do Elefante (MOEL), Morro do Cerrito (MOCE)
region of Rio Grande do Sul. Studies with various e Campus da Universidade Federal de Santa Maria
groups of animals, such as butterflies (Link et al. (UFSM). Um total de 19.699 indivíduos de 33 espécies
1977, Schwartz and Di Mare 2001, Dessuy and foi coletado; Canthidium aff. trinodosum Boheman,
Morais 2007, Sackis and Morais 2008), crustaceans 1858, Canthon latipes Blanchard, 1845, Dichotomius
(Bond-Buckup and Buckup 1994, Santos 2002), assifer (Eschscholtz 1822), Eurysternus caribaeus
reptiles (Santos et al. 2005), anurans (Santos et al. (Herbst 1789), Canthidium sp. e Canthon lividus
2008a), birds (Cechin et al. 2009), and mammals Blanchard, 1845 foram as espécies mais abundantes.
(Cáceres et al. 2007, Santos et al. 2008b), have shown MOEL apresentou a maior riqueza, MOCE a maior
great richness and the ecological importance of the abundância, enquanto UFSM teve os menores valores de
region for the maintenance of species occurring in it riqueza e abundância. A maior similaridade (qualitativa
(Cechin et al. 2009). Therefore, future policy actions e quantitativa) ocorreu entre MOEL e MOCE, enquanto
will also have information on Scarabaeinae in relation a menor ocorreu entre MOCE e UFSM. Apenas 51% das
to selecting priority areas for preservation in the espécies foram comuns aos três fragmentos. A riqueza e
region, where human activity increasingly threatens a abundância de Scarabaeinae estiveram positivamente
the maintenance of natural ecosystems. This region, correlacionadas com a temperatura do ar. A riqueza
characterized by the encounter of two biomes is a dos fragmentos diminuiu conforme o menor tamanho
priority in terms of wildlife preservation, as it may e maior grau de perturbação da estrutura da vegetação.
be a site of species evolution, where evolutionary
Palavras-chave: Mata Atlântica, rola-bosta, sul do
processes such as speciation and coevolution can be
Brasil, riqueza de espécies, distribuição temporal.
preserved (Spector 2002).

ACKNOWLEDGMENTS REFERENCES

We would like to thank the owners of the private ALMEIDA SSP AND LOUZADA JNC. 2009. Estrutura da
comunidade de Scarabaeinae (Scarabaeidae: Coleoptera)
properties sampled for allowing the study, Franciéle em fitofisionomias do Cerrado e sua importância para a
Garcês for assistance during fieldwork, Suzane conservação. Neotrop Entomol 38: 32-43.
Saldanha for improving the English version of the ANDRESEN E. 2003. Effect of forest fragmentation on dung
beetle communities and functional consequences for plant
manuscript, Instituto Brasileiro do Meio Ambiente regeneration. Ecography 26: 87-97.
e dos Recursos Naturais Renováveis (IBAMA) for ANDRESEN E. 2008. Short-term temporal variability in the
granting the license for the collections, Coordenação abundance of tropical dung beetles. Ins Conserv Divers
1: 120-124.
de Aperfeiçoamento de Pessoal de Nível Superior ARNAUD P. 2002. Les Coléoptères du Monde, Phanaeini, vol. 28.
(CAPES) for providing the first author with the Canterbury: Hillside Books, England, 151 p.

An Acad Bras Cienc (2013) 85 (2)

694 PEDRO G. DA SILVA, FERNANDO Z. VAZ-DE-MELLO and ROCCO A. DI MARE

AUDINO LD, NOGUEIRA JM, SILVA PG, NESKE MZ, RAMOS CORDEIRO JLP AND HASENACK H. 2009. Cobertura vegetal
AHB, MORAES LP AND BORBA MFS. 2007. Identificação atual do Rio Grande do Sul. In: PILLAR VP ET AL.
dos coleópteros (Insecta: Coleoptera) das regiões de (Eds), Campos Sulinos – conservação e uso sustentável da
Palmas (município de Bagé) e Santa Barbinha (município biodiversidade, Brasília: Ministério do Meio Ambiente,
de Caçapava do Sul), RS. Bagé: Embrapa Pecuária Sul, Brasil, p. 285-299.
Brasil, 92 p. COSTA LP, LEITE YLR, FONSECA GAB AND FONSECA MT.
AUDINO LD, SILVA PG, NOGUEIRA JM, MORAES LP AND VAZ- 2000. Biogeography of South American Forest Mammals:
DE-MELLO FZ. 2011. Scarabaeinae (Coleoptera, Scarabaeidae)
Endemism and Diversity in the Atlantic Forest. Biotropica
32: 872-881.
de um bosque de eucalipto introduzido em uma região
originalmente campestre. Iheringia Sér Zool 101: 121-126. COSTA LP, LEITE YLR, MENDES SL AND DITCHFIELD AD.
2005. Conservação de mamíferos no Brasil. Megadiver-
AUSDEN M. 1996. Invertebrates. In: SUTHERLAND WJ (Ed),
sidade 1: 103-112.
Ecological census techniques: a handbook, Great Britain:
DAMBROS VS, EISINGER SM AND CANTO-DOROW TS. 2004.
The Bath Press Avon, UK, p. 139-177.
Leguminosae do Campus da Universidade Federal de
BEGON M, TOWNSEND CR AND HARPER JL. 2007. Ecologia: Santa Maria, Rio Grande do Sul, Brasil. Ciência e Natura
de indivíduos a ecossistemas, 4th ed., Porto Alegre: 26: 43-60.
Artmed, Brasil, 752 p. DAVIS AJ, HOLLOWAY JD, HUIJBREGTS H, KRIKKEN J, KIRK-
BENCKE GA. 2009. Diversidade e conservação da fauna dos SPRIGGS AH AND SUTTON SL. 2001. Dung beetles as
campos do sul do Brasil. In: PILLAR VP ET AL. (Eds), indicators of change in the forests of northern Borneo. J
Campos Sulinos – conservação e uso sustentável da Appl Ecol 38: 593-616.
biodiversidade, Brasília: Ministério do Meio Ambiente, DAVIS AL, SCHOLTZ CH, DOOLEY P, BHAM N AND KRYGER
Brasil, p. 101-121. U. 2004. Scarabaeine dung beetles as indicators of
BILENCA DN AND MIÑARRO F. 2004. Identificación de Áreas biodiversity, habitat transformation and pest control
Valiosas de Pastizal (AVPs) en las Pampas y Campos chemicals in agro-ecosystems. S Afr J Sci 100: 415-424.
de Argentina, Uruguay y sur de Brasil. Buenos Aires: DAVIS ALV. 1996. Habitat associations in a South African,
Fundación de la Vida Silvestre, Argentina, 352 p. summer rainfall, dung beetle community (Coleoptera:
BOND-BUCKUP G AND BUCKUP L. 1994. A família Aeglidae Scarabaeidae, Aphodiidae, Staphylinidae, Histeridae,
(Crustacea, Decapoda, Anomura). Arq Zool 32: 159-347. Hydrophilidae). Pedobiologia 40: 260-280.
DAVIS ALV AND PHILIPS TK. 2005. Effect of deforestation on
BORNEMISSZA GF. 1976. The Australian dung beetle project,
a Southwest Ghana dung beetle assemblage (Coleoptera:
1965-1975. Aust Meat Res Comm Rev 30: 1-30.
Scarabaeidae) at the periphery of Ankasa conservation
BROWN-JrJ KS. 1991. Conservation of Neotropical environments: area. Environ Entomol 34: 1081-1088.
insects as indicators. In: Collins NM and Thomas JA DAVIS ALV, SCHOLTZ CH AND CHOWN SL. 1999. Species
(Eds), The conservation of insects and their habitats: turnover, community boundaries and biogeographical com-
15th Symposium of the Royal Entomological Society of position of dung beetle assemblages across an altitudinal
London, London: Academic Press, UK, p. 349-404. gradient in South Africa. J Biogeogr 26: 1039-1055.
BROWN-Jr KS. 1997. Diversity, disturbance, and sustainable DESSUY MB AND MORAIS ABB. 2007. Diversidade de borbo-
use of Neotropical forests: insects as indicators for letas (Lepidoptera, Papilionoidea e Hesperioidea) em
conservation monitoring. J Ins Conserv 1: 25-42. fragmentos de Floresta Estacional Decidual em Santa Maria,
BROWN-Jr KS AND FREITAS AVL. 2000. Atlantic Forest Rio Grande do Sul, Brasil. Rev Bras Zool 24: 108-120.
butterflies: indicators for landscape conservation. DOUBE BM. 1991. Dung beetle of Southern Africa. In:
Biotropica 32: 934-956. HANSKI I AND CAMBEFORT Y (Eds), Dung beetle
CÁCERES NC, CHEREM JJ AND GRAIPEL ME. 2007. Distribuição ecology, Princeton: Princeton University Press, USA,
geográfica de mamíferos terrestres na Região Sul do p. 133-155.
Brasil. Ciência & Ambiente 35: 167-180. EDMONDS WD. 2000. Revision of the Neotropical dung
beetle genus Sulcophanaeus (Coleoptera: Scarabaeidae:
CAMBEFORT Y AND HANSKI I. 1991. Dung beetle population
Scarabaeinae). Folia Heyrov Suppl 6: 1-60.
biology. In: HANSKI I AND CAMBEFORT Y (Eds),
ENDRES AA, CREÃO-DUARTE AJ AND HERNÁNDEZ MIM.
Dung beetle ecology, Princeton: Princeton University
2007. Diversidade de Scarabaeidae s. str. (Coleoptera)
Press, USA, p. 36-50.
da Reserva Biológica Guaribas, Mamanguape, Paraíba,
CECHIN SZ, MORAIS ABB, CÁCERES NC, SANTOS S, KOTZIAN Brasil: uma comparação entre Mata Atlântica e Tabuleiro
CB, BEHR ER, ARRUDA JS AND DELLA-FLORA F. 2009. Nordestino. Rev Bras Entomol 51: 67-71.
Fauna de Santa Maria. Ciência & Ambiente 38: 113-144. ESCOBAR F, HALFFTER G AND ARELLANO L. 2007. From forest
COLWELL RK. 2004. EstimateS: Statistic estimation of species to pasture: an evaluation of the influence of environment
richness and shared species from samples. Version 7.0. and biogeography on the structure of dung beetle
Available at: http://viceroy.eeb.uconn.edu/EstimateS. (Scarabaeinae) assemblages along three altitudinal gradients
Accessed on 15 November 2004. in the Neotropical region. Ecography 30: 193-208.

An Acad Bras Cienc (2013) 85 (2)

 DIVERSITY AND SEASONALITY OF DUNG BEETLES 695

FAVILA M AND HALFFTER G. 1997. The use of indicator groups HANSKI I AND CAMBEFORT Y. 1991. Competition in dung
for measuring biodiversity as related to community beetles. In: HANSKI I AND CAMBEFORT Y (Eds),
structure and function. Acta Zool Mex 72: 1-25. Dung beetle ecology, Princeton: Princeton University
FEARNSIDE PM. 2005. Desmatamento na Amazônia brasileira: Press, USA, p. 305-329.
história, índices e conseqüências. Megadiversidade 1: HERNÁNDEZ MIM. 2007. Besouros escarabeíneos (Coleoptera:
113-123. Scarabaeidae) da Caatinga paraibana, Brasil. Oecologia
FILGUEIRAS BKC, LIBERAL CN, AGUIAR CDM, HERNÁNDEZ Brasiliensis 11: 356-364.
MIM AND IANNUZZI L. 2009. Attractivity of omnivore, HERNÁNDEZ MIM AND VAZ-DE-MELLO FZ. 2009. Seasonal
carnivore and herbivore mammalian dung to Scarabaeinae and spatial species richness variation of dung beetle
(Coleoptera, Scarabaeidae) in a tropical Atlantic Forest (Coleoptera, Scarabaeidae s. str.) in the Atlantic Forest of
remnant. Rev Bras Entomol 53: 422-427. southeastern Brazil. Rev Bras Entomol 53: 607-613.
FLECHTMANN CAH AND RODRIGUES SR. 1995. Insetos
HULBERT SH. 1971. Nonconcept of species diversity: A cri-
fimícolas associados a fezes bovinas em Jaraguá do Sul/
tique and alternative parameters. Ecology 52: 577-586.
SC. 1. Besouros coprófagos (Coleoptera: Scarabaeidae).
Rev Bras Entomol 39: 303-309. INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. 2009.
Mapas Interativos: Biomas. Disponível em: http://mapas.
GARDNER TA, HERNÁNDEZ MIM, BARLOW B AND PERES CA.
2008. Understanding the biodiversity consequences of ibge.gov.br/biomas2/viewer.htm. Accessed on 28 June 2009.
habitat change: the value of secondary and plantation forests INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. 2010.
for Neotropical dung beetles. J Appl Ecol 45: 883-893. Cidades: Santa Maria, RS. Available at: http://www.ibge.
GÉNIER F. 2009. Le genre Eurysternus Dalman, 1824 gov.br/cidadesat/painel/painel.php?codmun=431690.
(Scarabaeidae: Scarabaeinae: Oniticellini), revision taxo- Accessed on 13 August 2010.
nomique et clés de determination illustrées. Sofia: Pensoft, INSTITUTO NACIONAL DE METEOROLOGIA. 2010. Gráficos –
Bulgary, 430 p. Estação Santa Maria, RS. Available at: http://www.inmet.
GILL BD. 1991. Dung beetles in tropical American forests. gov.br/html/observacoes.php?lnk=Graficos. Accessed on
In: HANSKI I AND CAMBEFORT Y (Eds), Dung beetle 04 September 2010.
ecology, Princeton, Princeton University Press, USA, INVENTÁRIO FLORESTAL CONTÍNUO. 2010. Inventário Florestal
p. 211-229. Contínuo – RS. Available at: http://coralx.ufsm.br/ifcrs/
GIULIETTI AM, HARLEY RM, QUEIROZ LP, WANDERLEY MGL index.php. Accessed on 16 August 2010.
AND VAN-DEN-BERG C. 2005. Biodiversidade e conser- KLEIN BC. 1989. Effects of forest fragmentation on dung and
vação das plantas no Brasil. Megadiversidade 1: 52-61. carrion beetle communities in central Amazonia. Ecology
HALFFTER G. 1991. Historical and ecological factors determi- 70: 1715-1725.
ning the geographical distribution of beetles (Coleoptera: KOLLER WW, GOMES A, RODRIGUES SR AND GOIOZO PFI.
Scarabaeidae: Scarabaeinae). Folia Entomol Mex 82: 2007. Scarabaeidae e Aphodiidae coprófagos em pastagens
195-238. cultivadas em área do cerrado sul-mato-grossense. Rev
HALFFTER G. 2005. Towards a culture of biodiversity Bras Zooc 9: 81-93.
conservation. Acta Zool Mex 21: 133-153.
LARSEN TH AND FORSYTH A. 2005. Trap spacing and
HALFFTER G AND ARELLANO L. 2002. Response of dung transect design for dung beetle biodiversity studies.
beetles diversity to human-induced changes in a tropical
Biotropica 37: 322-325.
landscape. Biotropica 34: 144-154.
LINK D, BIEZANKO C, TARRAGÓ MF AND CARVALHO
HALFFTER G AND EDMONDS WD. 1982. The nesting
S. 1977. Lepidoptera de Santa Maria e arredores. II.
behavior of dung beetles (Scarabaeinae): An ecologic and
Morphidae e Brassolidae. Rev Centro Ciências Rurais
evolutive approach. Mexico D.F.: Man and Biosphere
Program UNESCO, Mexico, 177 p. 7: 381-389.
HALFFTER G AND FAVILA ME. 1993. The Scarabaeidae (Insecta: LOBO JM, MARTÍN-PIERA F AND VEIGA CM. 1988. Las
Coleoptera) an animal group for analyzing, inventorying trampas pitfall con sebo, sus posibilidades en el estudio de
and monitoring biodiversity in tropical rainforest and las comunidades coprófagas de Scarabaeoidea (Col.). I.
modified landscapes. Biol Int 27: 15-21. Características determinantes de su capacidad de captura.
HALFFTER G, FAVILA ME AND HALFFTER V. 1992. A compa- Rev Ecol Biol Sol 25: 77-100.
rative study of the structure of the scarab guild in Mexican LOPES J, CHOCHON I, YUZAWA SK AND KURNLEIN RRC.
tropical rain forests and derived ecosystems. Folia 1994. Entomofauna do Parque Estadual Mata dos Godoy:
Entomol Mex 84: 131-156. II. Scarabaeidae (Coleoptera) coletados em armadilhas de
HALFFTER G AND MATTHEWS EG. 1966. The natural history solo. Semina 15: 121-127.
of dung beetles of the subfamily Scarabaeinae (Coleoptera: LOPES J, KORASAKI V, CATELLI LL, MARÇAL VVM AND
Scarabaeidae). Folia Entomol Mex 12/14: 1-312. NUNES MPBP. 2011. A comparison of dung beetle assem-
HAMMER O, HARPER DAT AND RYAN PD. 2001. PAST: blage structure (Coleoptera: Scarabaeidae: Scarabaeinae)
Palaeontological Statistics software package for education between an Atlantic forest fragment and adjacent
and data analysis. Palaeont Electr 4: 1-9. abandoned pasture in Paraná, Brazil. Zoologia 28: 72-79.

An Acad Bras Cienc (2013) 85 (2)

696 PEDRO G. DA SILVA, FERNANDO Z. VAZ-DE-MELLO and ROCCO A. DI MARE

LOUZADA JNC AND LOPES FS. 1997. A comunidade de MORENO CF. 2001. Métodos para medir la biodiversidad,
Scarabaeidae copro-necrófagos (Coleoptera) de um frag- MandT-Manuales and Tesis SEA. vol. 1. Zaragoza: Gorfi,
mento de Mata Atlântica. Rev Bras Entomol 41: 117-121. Zaragoza, Spain, 84 p.
LOUZADA JNC, LOPES FS AND VAZ-DE-MELLO FZ. 2007. MOURA LA. 2003. Coleópteros. In: FONTANA CS ET AL.
Structure and composition of a dung beetle community (Eds), Livro Vermelho da Fauna Ameaçada de no Rio
(Coleoptera, Scarabaeinae) in a small forest patch from Grande do Sul, Porto Alegre: EDIPUCRS, Brasil, p. 85-94.
Brazilian Pantanal. Rev Bras Zooc 9: 199-203. MOURA LA. 2007. Coleópteros terrestres. In: BECKER FG
LOUZADA JNC AND SILVA PRC. 2009. Utilisation of introduced ET AL. (Eds), Biodiversidade. Regiões da Lagoa do
Brazilian pastures ecosystems by native dung beetles: Casamento e dos Butiazais de Tapes, planície costeira
diversity patterns and resource use. Ins Conserv Divers do Rio Grande do Sul, Brasília: Ministério do Meio
2: 45-52. Ambiente/Fundação Zoobotânica do Rio Grande do Sul,
MACHADO PFS AND LONGHI SJ. 1990. Aspectos florísticos e Brasil, p. 210-229.
fitossociológicos do “Morro do Elefante”, Santa Maria, MYERS N, MITTERMEIER RA, MITTERMEIER CG, FONSECA
RS. Rev Centro Ciências Rurais 20: 261-280. GAB AND KENT J. 2000. Biodiversity hotspots for conser-
MADRUGA PRA, ILLANA VB, KLEINPAUL JJ, SCAPINI GP, vation priorities. Nature 403: 853-858.
BERGER G AND SALBEGO AG. 2007. Quantificação da NICHOLS E, LARSEN T, SPECTOR S, DAVIS AL, ESCOBAR F,
cobertura florestal do campus da Universidade Federal de FAVILA M AND VULINEC K. 2007. Global dung beetle
Santa Maria, com o auxílio de imagem de alta resolução. response to tropical forest modification and fragmentation:
Ambiência 3: 79-88. A quantitative literature review and meta-analyses. Biol
MAGURRAN AE. 1988. Ecological diversity and its measure- Conserv 137: 1-19.
ment. New Jersey: Princeton University Press, USA, 192 p.
NICHOLS E, SPECTOR S, LOUZADA J, LARSEN T, AMEZQUITA
MARCHIORI JNC. 2009. A vegetação em Santa Maria. Ciência S AND FAVILA ME. 2008. Ecological functions and
& Ambiente 38: 93-112. ecosystem services provided by Scarabaeinae dung
MARQUES AAB, FONTANA CS, VÉLEZ E, BENCKE GA, beetles. Biol Conserv 141: 1461-1474.
SCHNEIDER M AND REIS RS. 2002. Lista de Referência OVERBECK GE, MÜLLER SC, FIDELIS A, PFADENHAUER J,
da Fauna Ameaçada de Extinção no Rio Grande do Sul, PILLAR VP, BLANCO CC, BOLDRINI II, BOTH R AND
Decreto nº 41.672, de 10 de junho de 2002. Porto Alegre:
FORNECK ED. 2009. Os Campos Sulinos: um bioma
FZB/MCT-PUCRS/PANGEA, Brasil, 52 p.
negligenciado. In: PILLAR VP ET AL. (Eds), Campos
MARTÍNEZ NJ, GARCÍA H, PULIDO LA, OSPINO D AND Sulinos – conservação e uso sustentável da biodiversidade,
NARVÁEZ JC. 2009. Escarabajos coprófagos (Coleoptera: Brasília: Ministério do Meio Ambiente, Brasil, p. 24-41.
Scarabaeinae) de la Vertiente Noroccidental, Sierra
PECK SB AND FORSYTH A. 1982. Composition, structure, and
Nevada de Santa Marta, Colombia. Neotrop Entomol 38:
competitive behaviour in a guild of Ecuadorian rain
708-715.
forest dung beetles (Coleoptera, Scarabaeidae). Can J Zool
MATAVELLI RA AND LOUZADA JNC. 2008. Invasão de áreas
60: 1624-1634.
de savana intra-amazônicas por Digitonthophagus gazella
PELL MC, FINLAYSON BL AND MCMAHON TA. 2007. Updated
(Fabricius, 1787) (Insecta: Coleoptera: Scarabaeidae).
Acta Amazonica 38: 153-158. world map of the Köppen-Geiger climate classification.
Hydrol Earth Syst Sci 11: 1633-1644.
MCGEOCH MA, RENSBURG BJV AND BOTES A. 2002. The
verification and application of bioindicators: a case study PEREIRA PRB, GARCIA-NETTO LR, BORIN CJA AND
of dung beetles in a savanna ecosystem. J Appl Ecol SARTORI MGB. 1989. Contribuição à geografia física do
39: 661-672. município de Santa Maria: unidades de paisagem. Geogr
MEDRI IM AND LOPES J. 2001. Scarabaeidae (Coleoptera) do Ens Pesq 3: 37-68.
Parque Estadual Mata dos Godoy e de área de pastagem, ROESCH LFW, VIEIRA FCB, PEREIRA VA, SCHÜNEMANN AL,
no norte do Paraná, Brasil. Rev Bras Zool 18: 135-141. TEIXEIRA IF, SENNA AJT AND STEFENON VM. 2009. The
MILHOMEM MS, VAZ-DE-MELLO FZ AND DINIZ IR. 2003. Brazilian Pampa: a fragile biome. Diversity 2009: 182-198.
Técnicas de coleta de besouros copronecrófagos no SACKIS GD AND MORAIS ABB. 2008. Borboletas (Lepidoptera:
Cerrado. Rev Agropec Bras 38: 1249-1256. Hesperioidea e Papilionoidea) do campus da Universidade
MITTERMEIER RA, GIL PR, HOFFMANN M, PILGRIM J, Federal de Santa Maria, Rio Grande do Sul. Biota Neotrop
BROOKS T, MITTERMEIER CG, LAMOREUX J AND FONSÌA 8: 151-158.
GAB. 2005. Hotspots revisited: earth’s biologically richest SANTOS S. 2002. Crustáceo. In: ITAQUI J (Ed), Quarta
and most endangered terrestrial ecoregions. Mexico D.F.: Colônia de imigração Italiana: Inventários Técnicos. Flora
CEMEX, Mexico, 392 p. e Fauna, Santa Maria: Condesus Quarta Colônia, Brasil,
MORELLI E, GONZÁLEZ-VAINER P AND BAZ A. 2002. p. 193-198.
Coprophagous beetles (Coleoptera: Scarabaeoidea) in SANTOS TG, KOPP KL, SPIES MR, TREVISAN R AND CECHIN S.
Uruguayan Prairies: abundance, diversity and seasonal 2005. Répteis do campus da Universidade Federal de
occurrence. St Neotropl Fauna Environ 37: 53-57. Santa Maria, RS, Brasil. Biota Neotrop 5: 1-8.

An Acad Bras Cienc (2013) 85 (2)

 DIVERSITY AND SEASONALITY OF DUNG BEETLES 697

SANTOS TG, KOPP K, SPIES MR, TREVISAN R AND CECHIN S. SPECTOR S AND FORSYTH AB. 1998. Indicator taxa for biodi-
2008a. Distribuição temporal e espacial de anuros em versity assessment in the vanishing tropics. In: MACE
área de Pampa, Santa Maria, RS. Iheringia, Sér Zool 98: GM ET AL. (Eds), Conservation in a Changing World,
244-253. Cambridge: Cambridge University Press, UK, p. 181-209.
SANTOS TG, SPIES MR, KOPP K, TREVISAN R AND CECHIN S. TABARELLI M, PINTO LP, SILVA JMC, HIROTA MM AND
2008b. Mamíferos do campus da Universidade Federal BEDÊ LC. 2005. Desafios e oportunidades para a conser-
de Santa Maria, Rio Grande do Sul, Brasil. Biota Neotrop vação da biodiversidade na Mata Atlântica. Megadiversidade
8: 125-131. 1: 132-138.
SCHOOLMEESTERS P, DAVIS ALV, EDMONDS WD, GILL B, VAZ-DE-MELLO FZ. 1999. Scarabaeidae s. str. (Coleoptera:
MANN D, MORETTO P, PRICE D, REID C, SPECTOR S Scarabaeoidea) de um fragmento de Floresta Amazônica
AND VAZ-DE-MELLO FZ. 2010. ScarabNet Global Taxon no estado do Acre, Brasil. I. Taxocenose. An Soc Entomol
Database (version 1.5). Available at: http://216.73.243.70/ Brasil 28: 447-453.
scarabnet/results.htm. Accessed on 16 August 2010. VAZ-DE-MELLO FZ. 2000. Estado de conhecimento dos
SCHWARTZ G AND DI MARE RA. 2001. Diversidade de quinze Scarabaeidae s. str. (Coleoptera: Scarabaeoidea) do Brasil.
espécies de borboletas (Lepidoptera, Papilionidae) em sete In: MARTÍN-PIERA F ET AL. (Eds), Hacia un proyecto
comunidades de Santa Maria, RS. Ciência Rural 31: 49-55. CYTED para el inventario y estimación de la diversidad
SILVA PG. 2011. Dung beetles (Coleoptera: Scarabaeidae: entomológica en Iberoamérica, Zaragoza: Sociedad
Scarabaeinae) of two non-native habitats in Bagé, Rio Entomológica Aragonesa, Zaragoza, Spain, p. 181-195.
Grande do Sul, Brazil. Zool Stud 50: 546-559. VAZ-DE-MELLO FZ. 2007. Revision and phylogeny of the dung
SILVA PG, GARCIA MAR AND VIDAL MB. 2008. Besouros beetle genus Zonocopris Arrow 1932 (Coleoptera:
copronecrófagos (Coleoptera: Scarabaeidae stricto sensu) Scarabaeidae: Scarabaeinae), a phoretic of land snails.
coletados em ecótono natural de campo e mata em Bagé, Ann Soc Entomol Fr 43: 231-239.
RS. Ciência e Natura 30: 71-91. V AZ-DE-M ELLO FZ, EDMONDS WD , O CAMPO F AND
SILVA PG, GARCIA MAR AND VIDAL MB. 2009. Besouros SCHOOLMEESTERS P. 2011. A multilingual key to the
copro-necrófagos (Coleoptera: Scarabaeidae sensu stricto) genera and subgenera of the subfamily Scarabaeinae of
do município de Bagé, RS (Bioma Campos Sulinos). the New World. Zootaxa 2854: 1-73.
Biociências 17: 33-43. VAZ-DE-MELLO FZ AND GÉNIER F. 2009. Notes on the
SILVA PG, VAZ-DE-MELLO FZ AND DI-MARE RA. 2012. behavior of Dendropaemon Perty and Tetramereia Klages
Attractiveness of different bait to the Scarabaeinae (Scarabaeidae: Scarabaeinae: Phanaeini). Coleopt Bull
(Coleoptera: Scarabaeidae) in forest fragments in extreme 63: 364-366.
southern Brazil. Zool Stud 51: 429-441. VAZ-DE-MELLO FZ, GÉNIER F AND SMITH ABT. 2010.
SILVEIRA-NETO S, NAKANO O, BARBIN D AND VILLA-NOVA Reclassification of Homocopris Burmeister as a valid genus
NA. 1976. Manual de Ecologia dos Insetos. São Paulo: to accommodate three species formerly in Dichotomius
Agronômica Ceres, Brasil, 419 p. Hope (Scarabaeidae: Scarabaeinae: Coprini). Coleopt Bull
SIMMONS LW AND RIDSDILL-SMITH TJ. 2011. Reproductive 64: 192-192.
competition and its impact on the evolution and ecology VAZ-DE-MELLO FZ, LOUZADA JNC AND SCHOEREDER JH.
of dung beetles. In: SIMMONS LW AND RIDSDILL- 1998. New data and comments on Scarabaeidae (Coleoptera:
SMITH TJ (Eds), Ecology and evolution of dung beetles, Scarabaeoidea) associated with Attini (Hymenoptera:
Oxford: Blackwell Publishing Ltd., UK, p. 1-20. Formicidae). Coleopt Bull 52: 209-216.
SPECTOR S. 2002. Biogeographic crossroads as priority areas VERDÚ JR, MORENO CE, SÁNCHEZ-ROJAS G, NUMA C,
for biodiversity conservation. Conserv Biol 16: 1480-1487. GALANTE E AND HALFFTER G. 2007. Grazing promotes
SPECTOR S. 2006. Scarabaeine dung beetles (Coleoptera: dung beetle diversity in the xeric landscape of a Mexican
Scarabaeidae: Scarabaeinae): an invertebrate focal taxon Biosphere Reserve. Biol Conserv 140: 308-317.
for biodiversity research and conservation. Coleopt Bull WATERHOUSE DF. 1974. The biological control of dung.
5: 71-83. Sci Am 230: 100-109.
SPECTOR S AND AYZAMA S. 2003. Rapid turnover and edge WOLDA H. 1988. Insect seasonality: Why? Ann Rev Ecol Syst
effects in dung beetle assemblages (Scarabaeidae) at a 19: 1-18.
Bolivian Neotropical forest-savanna ecotone. Biotropica
35: 394-404.

An Acad Bras Cienc (2013) 85 (2)