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The Role of Body Size and Shape in
Understanding Competitive Interactions within a
Community of Neotropical Dung Beetles
Article in Journal of Insect Science · February 2011
DOI: 10.1673/031.011.0113 · Source: PubMed
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Journal of Insect Science:Vol. 11 | Article 13
Hernández et al.
The role of body size and shape in understanding competitive
interactions within a community of Neotropical dung beetles
Malva I. M. Hernández1a, Leandro R. Monteiro2b, and Mario E. Favila3c
1
Departamento de Ecologia e Zoologia, Universidade Federal de Santa Catarina, Caixa Postal 476, Florianópolis,
SC, Brazil 88010-970
2
Department of Biological Sciences, The University of Hull, Hull, HU6 7RX, United Kingdom
3
Instituto de Ecología A.C., Apartado Postal 63, Xalapa, 91000, Veracruz, Mexico
Abstract
Geometric morphometrics is helpful for understanding how body size and body shape influence
the strength of inter-specific competitive interactions in a community. Dung beetles,
characterized by their use of decomposing organic material, provide a useful model for
understanding the structuring of ecological communities and the role of competition based on
their size and morphology. The relationship between body size and shape in a dung beetle
community from the Atlantic Forest in Serra do Japi, Brazil was analyzed for 39 species. Fifteen
anatomical landmarks on three-dimensional Cartesian coordinates were used to describe both the
shape and the size of the body of each species on the basis of the centroid located along
homologous points in all of the species. The first vector of a principal components analysis
explained 38.5% of the morphological variation among species, and represents a gradient of body
shape from elongated, flattened bodies with narrow abdomen to rounded or convex bodies. The
second component explained 17.8% of the remaining variation in body shape, which goes from
species with an abdomen that is larger than the elytra to species with constricted abdomens and
large elytra. The relationship between body size and shape was analyzed separately for diurnal
and nocturnal species. In both guilds not only were there differences in body size, but also in
body shape, suggesting a reduction in their level of competition.
Keywords: Brazil, Coleoptera, geometric morphometrics, inter-specific competition, Scarabaeinae
Correspondence: a malvamh@ccb.ufsc.br, b L.Monteiro@hull.ac.uk, c mario.favila@inecol.edu.mx
Received: 21 June 2009, Accepted: 3 November 2009
Copyright : This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits
unrestricted use, provided that the paper is properly attributed.
ISSN: 1536-2442 | Vol. 11, Number 13
Cite this paper as:
Hernández MIM, Monteiro LR, Favila ME. 2011. The role of body size and shape in understanding competitive
interactions within a community of Neotropical dung beetles. Journal of Insect Science 11:13 available online:
insectscience.org/11.13
Journal of Insect Science | www.insectscience.org
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Journal of Insect Science:Vol. 11 | Article 13
Hernández et al.
Introduction
Species morphology has always been
considered an important factor that affects the
patterns of inter- and intra-specific
competition in ecological communities.
Within a single community, species from the
same taxonomic group that have a similar
body size often exploit similar resources and
are therefore likely to compete more strongly
with each other than with species which are
less similar (Warren and Lawton 1987;
Juliano and Lawton 1990). According the
principle of competitive exclusion two species
cannot occupy the same ecological niche
(Gause 1934). However, resource partitioning
should reduce competition and allow for
species coexistence (Begon et al. 1996;
Tilman 2007). Animals with different body
shapes supposedly exploit some resources
more efficiently than other species do, and
this reduces competition and promotes species
coexistence (Hutchinson & MacArthur 1959).
Body size and shape are often correlated with
various other individual traits such as
physiology, behavior, and metabolism (e.g.
life expectancy, locomotion, and fecundity),
as well as ecological characteristics such as
population density, the distribution of relative
species abundance, and competitive ability
(Peters 1983; Calder 1984; Schmidt-Nielsen
1984; Morse et al. 1988; Lawton 1991;
Blackburn and Gaston 1997). Although
coexistence is often attributed to interspecific
differences in morphology, direct evidence is
relatively rare (Gurd 2007).
Developments in geometric morphometrics
have been successful in combining the fields
of geometry, biology, and statistics for the
purpose of doing more reliable comparative
studies (Bookstein 1982, 1991; Rohlf and
Marcus 1993). Insects are ideal for this type of
Journal of Insect Science | www.insectscience.org
study, not only because of their
hyperabundance, but also because they
possess a well defined exoskeleton (see
Adams and Funk 1997; Pretorius et al. 2000;
Pretorius and Scholtz, 2001). Within the
insects, beetles generally have an oval or
elongated shape and a convex body. Their
robust exoskeleton makes measuring them a
straightforward task. Additionally, the
complete metamorphosis that occurs in beetles
reduces the difficulty presented by allometric
growth in immature stages, as measurements
are limited to adult beetles.
The species of the subfamily Scarabaeinae
(Scarabaeidae), commonly known as dung
beetles, are characterized by the use of
decomposing organic material by adults and
larvae as a food source. There are 25 to 70
species in tropical rain forests, but as many as
124 species in African savannas (Favila and
Halffter
1997).
Several
etoecological
differences have been invoked to explain the
high diversity of dung beetle species in
tropical ecosystems: food relocation system
with burying, roller, and dweller species; diel
activity including nocturnal, crepuscular, and
diurnal species; food preference with
coprophagous,
copronecrophagous,
and
necrophagous species; and finally there are
stenotopic and eurytopic species with different
temporal activity patterns over an annual
period (Halffter and Matthews 1966; Hanski
and Koskela 1977; Halffter and Edmonds
1982; Giller and Doube 1989, 1994; Hanski
and Cambefort 1991; Halffter et al. 1992;
Davis 1996; Palestrini et al. 1998; Hernández
2002; Feer and Pincebourde 2005; Horgan
and Fuentes 2005). The reduction in direct
competition and the resulting coexistence of
many species is expected to result from not
only these etoecological differences, but also
from morphometric variations. As such, dung
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Journal of Insect Science:Vol. 11 | Article 13
Hernández et al.
beetles seem to be an ideal group for
analyzing how morphology is related to niche
segregation, resource partitioning, and the
structuring of communities.
This paper presents an approach that uses
geometric morphometrics to elucidate the
competitive relationships in dung beetle
assemblages in order to understand
community structure and species coexistence.
We predict that similar sized species will have
different shapes where they overlap along
some major resource continuum, and that sizeshape overlap will be low within nocturnal or
diurnal species.
Materials and Methods
Dung beetles were collected in an Atlantic
Forest in the Serra do Japi, São Paulo, Brazil
(23°12’ to 23°22’ S and 46°53’ to 47°03’ W)
at an altitude of 1000 MASL. Sampling was
carried out between September 1997 and
August 1998 at 6 different sites using 4 pitfall
traps per site (a total of 24 pitfall traps) that
were baited with human feces and left open
for two days every month. Throughout the
sampling period, 3524 individuals belonging
to 39 species of Scarabaeinae were captured
(Table 1). A total of 917 specimens were
measured, usually 50 individuals per species,
but for less abundant species all of the
captured
individuals
were
measured.
Specimens were deposited in the Museu de
Zoologia, Sao Paulo University and were
identified by Fernando Z. Vaz-de-Mello.
Geometric morphometric analyses
The Cartesian coordinates of anatomical
landmarks
are
used
in
geometric
morphometrics. These are specific locations
on the organism’s body, such as the points of
convergence of structures, the apices of
processes or their corresponding endpoints
Journal of Insect Science | www.insectscience.org
(Bookstein 1991). To study the difference in
shape between two or more bodies (as
described by landmark configurations), it is
first necessary to plot the coordinates of the
points as a figure in two or three-dimensional
space on Cartesian axes. The resulting figure
can then be thought of as a single point on a
system of orthogonal axes, the number of
which depends on the number of points that
each figure has. This multidimensional space
contains information about the shape, the size,
position, and orientation of the body
(Monteiro and Reis 1999).
To compare the shapes of two species’
configurations, it is necessary to remove the
information that does not pertain to shape,
which means removing information about
size, position, and orientation (Bookstein
1989). To eliminate the effect of size, the
species configurations are scaled, making the
centroid size of the figures equal to one. The
centroid represents the species configuration
midpoint or the centre of gravity of the figure,
and its size is defined as the square root of the
sum of the squares of the distances among
each point of the species configuration and the
centroid (Bookstein 1991). To eliminate the
effects of position, the species configurations
are translated to the same position in space,
superimposing the centroid of one figure upon
the centroid of another. The effect of
orientation is eliminated by rotating the
figures, following a criterion of optimization
that minimizes the sum of the squares of the
distances between homologous points, such
that the rotation results in the minimum
distance between the points of one over those
of the other (Rohlf and Slice 1990).
Data collection
Fifteen anatomical landmarks were selected
on three-dimensional Cartesian coordinates to
describe both the shape of the species and the
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Journal of Insect Science:Vol. 11 | Article 13
Hernández et al.
size of the centroid. The following landmarks
were chosen along homologous points in all
the species: 1) anterior margin of the head; 2)
eye position; 3) division between the
pronotum and the elytra; 4) division between
the thorax and the abdomen; 5) posterior
margin of the abdomen; 9) point of insertion
of the anterior legs; 10 and 11) points of
insertion of the central legs; 12) point of
insertion of the posterior legs; 13) anterior
point of convergence between elytra; 14)
central point (mid-line) of convergence
between elytra, and 15) posterior margin
(along mid-line) of the elytra. Points 6, 7, and
8 correspond to points 4, 3, and 2,
respectively, for the other side of the body.
The average shape of the body of dung beetles
is shown in three-dimensional space in Figure
1. The coordinates of this synthetic body-plan
were calculated from a global average based
on all 39 species, and were used as reference
points for describing the variation in shape
among individual species. The data points
were captured using a video camera and the
program MorphoSys (Meacham and Duncan
1993), and a stereoscopic microscope was also
used for individuals with a body length less
than 8 mm.
After eliminating the information pertaining to
size, position, and orientation, the residual
information was used to characterize the body
shape variables in a principal components
analysis (PCA). Shape differences among
species were visualized using icons
representing the gradients along the major
axes of variation. The similarities in shape
among species were subjected to a
hierarchical evaluation using the Procrustes
distance in morphometric space in a cluster
analysis with the Unweighted Pair-Group
Average (UPGMA) method.
Figure 1. Average body shape for a synthetic Scarabaeinae beetle based on the configuration of 15 body landmarks in threedimensional morphometric space. Landmark descriptions are given in Methods. The graphical representation of the body-plan
can be observed from any angle, thereby facilitating the understanding of variability in body shape. High quality figures are
available online.
Journal of Insect Science | www.insectscience.org
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Journal of Insect Science:Vol. 11 | Article 13
Hernández et al.
The size of each species was measured from
the size of the centroid (average of all sample
individuals) – a measurement that is
considered to be a geometrically robust
representation of the size of insects for which
morphology is often complex (Bookstein
1982, 1991). However, to allow for the
comparison of the results of this study with
those of other studies, body length was
measured as the distance from the anterior
margin of the head to the posterior edge of the
abdomen (the distance between points 1 and 5
of the landmark configurations).
The relationship between body size and body
shape was analyzed separately for diurnal and
nocturnal species. To this end, first the diel
activity was noted for each species according
to Hernández (2002), who identified the
diurnal and nocturnal species of the Serra do
Japi. Then, to visualize the relationship
between body size and body shape for each
guild, the size of each species (x axis) was
graphed in relation to the first PCA axis
obtained in the previous analysis. This
allowed direct comparison of differences in
body size and shape among the species which
supposedly compete more intensely at the
same time for the same resource.
Results
The principal components analysis revealed a
gradient which describes the greatest amount
of variation in body shape among species. The
first component explains 38.5% of the
variation in shape, and represents a gradient
between species which are elongated and
flattened with a narrow abdomen (negative
scores) and those with a rounded or convex
body shape (positive scores). The second
component explains 17.8% of the remaining
variation, and represents a gradient between
Journal of Insect Science | www.insectscience.org
species with an abdomen that is proportionally
larger than the elytra (negative scores) versus
species with proportionally large elytra but
constricted abdomens (positive scores, Figure
2).
The species with the lowest scores on the first
and second components belong to the genus
Eurysternus and these have the most
elongated shape and flattest bodies with a
narrow abdomen, but their abdomen is
proportionally larger than their elytra. The
species of the genus Deltochilum are more
gently elongated, as are those of Canthonella
sp.,
Paracanthon
pereirai,
and
Scybalocanthon nigriceps (Figure 2, see Table
1 for codes assigned to species). The species
of Uroxys (except U. aterrima) and Trichillum
are also more gently elongated, but as they
have the highest scores on the second
component, they have proportionally large
elytra
and
a
constricted
abdomen.
Coprophanaeus saphirinus and Phanaeus
splendidulus have high scores on the first
component, but low on the second component,
with rounded or convex body shapes and a
proportionally larger abdomen than elytra.
Species from the genera Dichotomius,
Canthidium, Canthon, and Onthophagus have
high scores on the first component and
increasing scores along the second
component, so they tend to have rounded
body shapes and large elytra with a
constricted abdomen. Ateuchus histrio,
Ontherus azteca, and Uroxys aterrima have
high scores on the first and second
components, with rounded or convex body
shapes and proportionally large elytra and a
constricted abdomen.
As a complement to the PCA, the cluster
analysis allowed a simultaneous evaluation of
all 15 morphological landmarks based on the
underlying similarity matrix for different
5
Journal of Insect Science:Vol. 11 | Article 13
Hernández et al.
Figure 2. Principal Components Analysis (PCA) illustrating differences in body shape for 39 species of Scarabaeinae. A visual
representation of the gradients in body shape along the principal axes is provided by two-dimensional sketch diagrams. High
quality figures are available online.
species (Figure 3). There was a tendency to
group species according to their taxonomy,
with closely related species clustering tightly
together. This pattern was most evident for
Eurysternus species which, due to their unique
shape, were grouped together in an isolated
cluster separate from all other species.
However, in spite of this general pattern, the
location of some species does not correspond
to their taxonomy. Some species from
different tribes have similar shapes, while
others from the same tribe have contrasting
shapes. Two large, but distinct taxonomic
groups were identified as having similar body
shapes (Figure 3). The first included all the
species of tribe Canthonini (except Canthon)
together with species of the genera Uroxys
and Trichillum (tribe Ateuchini, except U.
Journal of Insect Science | www.insectscience.org
aterrima). The second group included all
other species of Ateuchini, together with the
Coprini (Dichotomius, Ontherus) and
Phanaeini (Coprophanaeus, Phanaeus), as
well as all the species of the genus Canthon
(tribe Canthonini) (Figure 3). These results
concur with those of the PCA.
Measurements of body size (centroid size) and
body length are given in Table 1. There was a
positive and highly significant correlation (r2
= 0.998, p < 0.001) between body length and
the size of the centroid, represented by the
linear equation: centroid size = 0.031 + 1.247
x length.
The relationships between body size and body
shape (defined by the first principal
6
Journal of Insect Science:Vol. 11 | Article 13
Hernández et al.
component) show that the 19 diurnal species
were divided into two major groups as defined
Table 1. Species of Scarabaeinae captured in the Atlantic Forest at the Serra do Japi, Brazil. Body size is defined by the size of the centroid.
Species
Code
n
Body Size
(cm)
S. D.
Body Length
(cm)
S. D.
A. P
Ateuchus near histrio (Balthasar, 1939)
atehis
3
0.885
0.0378
0.651
0.0449
D
Canthidium dispar Harold, 1867
candis
1
1.259
-
0.983
-
D
Canthidium near sulcatum (Perty, 1830)
cansul
1
1.151
-
0.879
-
D
Canthidium trinodosum (Bohenann, 1858)
cantri
50
0.710
0.0483
0.537
0.0389
D
Canthidium sp.1
cansp1
4
0.762
0.0500
0.596
0.0381
D
Canthidium sp.2
cansp2
50
0.689
0.0640
0.526
0.0505
D
Trichillum sp.1
trisp1
17
0.481
0.2667
0.355
0.0201
-
Trichillum sp.2
trisp2
1
0.459
-
0.346
-
-
Uroxys aterrima Harold, 1867
uroate
16
1.119
0.1038
0.859
0.0907
N
Uroxys kratochvili Batlhasar, 1940
urokra
50
0.527
0.0288
0.393
0.0223
N
Uroxys lata Arrow, 1933
urolat
50
0.608
0.0322
0.451
0.0258
N
Uroxys sp.1
urosp1
20
0.365
0.0204
0.274
0.0175
N
Uroxys sp.2
urosp2
6
0.544
0.0251
0.409
0.0229
N
Dichotomius assifer (Eschscholtz, 1822)
dicass
50
2.210
0.1310
1.757
0.1123
N
Dichotomius bechynei Martínez, 1973
dicbec
4
1.899
0.2039
1.557
0.1750
N
Dichotomius carbonarius (Mannerheim, 1929)
diccar
2
2.243
0.1343
1.781
0.0948
N
Dichotomius depressicollis (Harold, 1867)
dicdep
3
2.650
0.0403
2.125
0.0506
N
Dichotomius mormon (Ljungh, 1799)
dicmor
11
2.889
0.2130
2.298
0.1939
N
Dichotomius sp.1
dicsp1
36
1.610
0.1110
1.267
0.0993
N
Dichotomius sp.2
dicsp2
2
1.962
0.0507
1.586
0.0339
N
Ontherus azteca Harold, 1869
ontazt
7
1.755
0.1479
1.367
0.1165
N
Eurysternus cyanescens Balthasar, 1939
eurcya
50
1.464
0.0673
1.192
0.0590
D
Eurysternus hirtellus Dalman, 1824
eurhir
28
0.938
0.0586
0.762
0.0522
D
Eurysternus parallelus Laporte, 1840
eurpar
6
1.452
0.0946
1.186
0.0755
D
Eurysternus sp.
eursp
50
1.839
0.1023
1.481
0.0823
D
Coprophanaeus saphirinus (Sturm, 1826)
copsap
7
2.322
0.2266
1.801
0.1652
D
Phanaeus splendidulus (Fabricius, 1781)
phaspl
6
2.264
0.0437
1.795
0.0289
D
Onthophagus sp.
ontsp
14
0.898
0.0483
0.706
0.0406
-
Canthon latipes Blanchard, 1843
canlat
50
1.220
0.0653
0.956
0.0569
D
Canthon rutilans Laporte, 1840
canrut
3
1.454
0.0991
1.168
0.0745
D
Canthon sp.
cansp
18
0.805
0.0506
0.617
0.0448
D
Canthonella sp.
cantsp
50
0.334
0.0215
0.248
0.0177
D
Deltochilum brasiliense (Laporte, 1840)
delbra
32
2.864
0.2248
2.191
0.1870
N
Deltochilum furcatum (Laporte, 1840)
delfur
50
2.158
0.1072
1.661
0.1027
N
Deltochilum morbillosum Burmeister, 1848
delmor
31
1.456
0.0660
1.126
0.0726
N
Deltochilum rubripenne (Gory, 1831)
delrub
50
1.626
0.0671
1.257
0.0676
D
Paracanthon pereirai d'Andretta & Martínez, 1957
parper
13
0.582
0.0363
0.446
0.0277
D
Scybalocanthon nigriceps (Harold, 1868)
scynig
50
1.182
0.0810
0.932
0.0719
D
Sylvicanthon foveiventre (Schmidt, 1920)
sylfov
25
0.907
0.0639
0.656
0.0616
Code = species code for PCA analyses, n = number of individuals measured, AP = activity pattern (D = diurnal, N = nocturnal).
N
Journal of Insect Science | www.insectscience.org
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Journal of Insect Science:Vol. 11 | Article 13
Hernández et al.
Figure 3. UPGMA cluster analysis based on a Procrustes distance matrix defining differences in body shape for 39 sympatric Scarabaeinae
species from Serra do Japi, Brazil. High quality figures are available online.
by differences in body shape, though there is
notable variability in size within each group
(Figure 4a). In addition, each species is
located at a unique coordinate as defined by
its size and morphology. A similar pattern was
found for the 17 nocturnal species, but the
range of body size was broader than that of
the diurnal species.
Additionally, nocturnal species have more
convex and bigger bodies than diurnal species
(Figure 4b). The species of Canthidium
(diurnal) and Uroxys (nocturnal) were
respectively grouped very closely together
Journal of Insect Science | www.insectscience.org
indicating very little variability in shape or
size within each genus.
Discussion
The assemblage of Scarabaeinae beetles in the
Serra do Japi is characterized by high levels of
diversity and abundance (Hernández and Vazde-Mello 2009) and, as results show, high
diversity in body size and morphology. This
structure is typical of other tropical dung
beetle assemblages (Halffter and Matthews
1966; Hanski 1991; Gill 1991; Halffter et al.
1992; Davis et al. 2001; Endres et al. 2007;
Gardner et al. 2008; Navarrete and Halffter
8
Journal of Insect Science:Vol. 11 | Article 13
2008),
and
competition
is
Hernández et al.
presumably
involved in their structuring (Hanski and
Figure 4. Relationship between body size (i.e. the size of the centroid in cm) and body shape (first principal component in the
PCA) in (a) the diurnal and (b) nocturnal dung beetle species in Serra do Japi, Brazil. High quality figures are available online.
Journal of Insect Science | www.insectscience.org
9
Journal of Insect Science:Vol. 11 | Article 13
Hernández et al.
Cambefort 1991). However, the few studies
conducted with dung beetles that have
experimentally analyzed competition under
field and laboratory conditions (Giller and
Doube 1986; Horgan and Fuentes 2005; Slade
et al. 2008), do not explicitly include the
morphology of the species in their analysis.
Based on the results presented here, the
incorporation of this approach, together with
species size, allows better understanding of
the role of species morphology in the intraand interspecific interactions that occur in
dung beetle assemblages.
Within a single community, species from the
same taxonomic group that have a similar
body size often exploit similar resources and
are therefore likely to compete more strongly
with each other than with species which are
less similar (Warren and Lawton 1987). In
Serra do Japi, the Scarabaeinae belonging to
the same genera and sharing a similar body
shape clustered together in both the principal
components and cluster analyses. This was
particularly evident for the species of
Eurysternus,
Canthidium,
Uroxys,
Dichotomius, the Phanaeus, and the roller
species
belonging
to
Canthon
and
Deltochilum, suggesting that competition
should be strong among these taxonomic
groups. However, although such similarities in
body shape suggest that the species of a genus
employ similar life history strategies to
exploit common resources, the fact that there
are differences in body size also suggest
asymmetric competition between species of
the same clade. In contrast to this general rule
there were clusters of species that were not
related at the genus level, but that shared
similar body shape. An example of this is the
group formed by Ontherus azteca, Atheuchus
histrio, and Uroxys aterrima. However, this
does not necessarily imply intense
competition between these species because
Journal of Insect Science | www.insectscience.org
they differ in body size and in their foraging
strategies.
There are two key limiting factors in relation
to the size of species within a given
community. Small individuals are limited by
their physical capacity to acquire resources,
but they are efficient at converting food into
reproductive output. In contrast, large
individuals are effective at securing resources,
but are much less effective at exploiting them
for reproduction. These two processes often
result in the evolution of an optimal size that
characterizes the majority of species (Brown
et al. 1993). There is considerable variation in
size in the assemblage of dung beetles in the
Serra do Japi (as defined by the centroid size),
ranging from the smallest species (e.g.,
Canthonella sp.) with a size of 3 mm to the
largest with an average body size of 3 cm
(Dichotomius mormon). However, the
centroid size of more than half (21) of the
coexisting 39 species was between 0.5 and 1.5
cm, suggesting that this is the optimal size
interval for the assemblage of dung beetles in
the Serra do Japi. These results also suggest
that the structure of the dung beetle
assemblage from the Serra do Japi mainly
reflects a variance-covariance dynamic; one in
which many species do not use up their
patchily available resources quickly, but
rather compete for them over a prolonged
period of time (see Hanski 1991).
The relationship found between body size and
body shape in this study revealed that some
species are very similar in body shape but
have marked differences in body size,
confirming predictions for both diurnal and
nocturnal species. This fact, together with the
etoecological differences among the cooccurring species of dung beetles from the
Serra do Japi may facilitate their coexistence,
and this is evident within and between diurnal
10
Journal of Insect Science:Vol. 11 | Article 13
Hernández et al.
and nocturnal species. In conclusion, the
geometric morphometric analysis suggests
that body size and body shape are important
factors that should be incorporated into
studies on the structure of dung beetle
assemblages. Alternative life history strategies
for exploiting common resources depend to a
large extent upon differences in body size and
body shape among species in the same
functional group and generate asymmetric
competitive
interactions.
Linking
the
behavior, body size, morphology, and life
history of dung beetles, as well as
phylogenetic and empirical studies, will help
achieve a better understanding of how dung
beetle assemblages are structured in natural
and disturbed ecosystems.
Begon M, JL Harper, CR Townsend. 1996.
Ecology, individuals, populations and
communities. Blackwell Scientific
Publications.
Acknowledgements
Bookstein FL. 1991. Morphometric Tools for
Landmark Data: Geometry and Biology.
Cambridge University Press.
The authors thank Dr. Sérgio F. dos Reis, Dr.
Woodruff W. Benson and Dr. Ricardo
Iglesias-Rios for supervising the first author’s
studies, Fernando Z. Vaz-de-Mello for species
identification, Toby A. Gardner for useful
comments on the manuscript, Jason Maté for
help with text translation, and Bianca Delfosse
for revising the English of the final version of
the ms. We also thank the Secretaria
Municipal de Educação de Jundiaí for
authorizing the study at Serra do Japi and the
Conselho Nacional de Desenvolvimento
Científico e Tecnológico for the scholarship
granted to the first author.
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