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Half Fter 2002
Half Fter 2002
ABSTRACT
This paper examines dung beetle communities in remnant patches of tropical deciduous forest at Veracruz, Mexico,
as a case study of the effects of tropical deforestation on biodiversity. The two study areas have a common biogeographic
history and similar macroclimatic conditions and have been modified by human activities to different extents. The
main difference between them is that cattle, which provide the dung beetle’s food supply, are present in only one of
the areas. Comparison of the dung beetle faunas sheds light on the relative importance of forest cover versus food
supply as the principal factor determining the structure and diversity of the fauna. This comparison, which we broaden
through an examination of data from other localities in central Veracruz, permits us to speculate about what happens
to biodiversity when a tropical deciduous forest undergoes modification of varying type and intensity. Where tree
cover has been most modified, native forest species undergo local extinction and are replaced by open area species.
On the whole, there has not been a net reduction in species richness (gamma diversity) in the fragmented landscape
of central Veracruz, although local species richness (alpha diversity) has diminished.
RESUMEN
En este trabajo se presenta una aproximacibn de lo que ocurre con la biodiversidad estudiada a travts de un grupo
indicador (10s escarabajos del estitrcol) en dos remanentes de bosque tropical caducifolio del estado de Veracruz,
Mtxico. Los dos sitios comparten la misma historia biogeografica, condiciones macroclimiticas semejantes, y ser
bosques parcialmente modificados por la actividad humana. La diferencia principal esti en la oferta de alimento para
10s Scarabaeinae, porque solamente en uno de 10s lugares hay ganado vacuno. L a comparacibn de la fauna de Scara-
baeinae de 10s dos lugares nos permite sefdar que la cubierta forestal, y no la oferta de alimento, es el principal
elemento conformador de la estructura y diversidad del gremio. Esta comparacibn, ampliada con datos de otros puntos
de Veracruz centro nos permite especular lo que ocurre con la biodiversidad (representada por 10s Scarabaeinae) al
modificarse el bosque tropical caducifolio en distintas formas e intensidades. Es relevante la sobrevivencia de las especies
propias del bosque a nivel paisaje (diversidad gama), aunque puedan desaparecer en parte a escala puntual. h i como
su reemplam por especies helibfilas en 10s puntos en que la vegetacibn arbbrea ha sido m&i modificada. En conjunto
el paisaje fragmentado y diverso de Veracruz centro no seiiala una ptdida de especies, aunque puntualmente (diversidad
alfa) si ocurra.
Kq word: biodivenity indicator groups; human disturbance; Mexico; Srarabaeinae; tropical deciduow $rest.
FEWPUBLICATIONS MEASURE BIODIVERSITY LOSS IN DIF- portant loss of biodiversity. There is no doubt that
FERENT TAXA, especially in the tropics, despite the this view (which has led to much speculation about
fact that much has been published about loss of the extinction of species) is realistic at the small
species due to human activities (Murphy 1989, spatial and temporal scales at which the changes
Brown & Brown 1992, Santos Filho 1995). Almost take place. These conclusions, however, may not be
all studies have aimed at determining the local ef- directly extrapolated to the landscape level, which
fects of habitat destruction (e.g., for arthropods, see is the scale at which extinction and survival gen-
Klein 1989, Shure & Phillips 1991, Holloway et erally occur (except in the case of restricted-range
af. 1992, Majer & Beeston 1996). The conclusions endemics).
of these studies are alarming: few species from the There are two main reasons why the conclu-
original communities survive and there is an im- sions of small-scale studies cannot be extrapolated
directly to the much larger scale of landscapes.
’Received 8 Mar 2000; revision accepted 10 March First, the physical matrix may be heterogeneous,
2001. especially in landscapes with complex topography.
E-mail: halfier@ecologia.edu.mx This heterogeneity (orographic, edaphologic) does
E-mail: lucreci@ecologia.edu.mx not permit human activities to occur uniformly
144
Dung Beetles and Tropical Deforestation 145
throughout the landscape. Second, not all human of large species and burrowers, greater total bio-
activities cause radical changes to natural commu- mass, and lower equitability.
nities. In the tropics, a forest may be destroyed over
a large area to provide land for plantations or for METHODS
livestock, but remnant patches are often left rela-
tively unmodified. In such cases, human activities STUDYAws.-The two study areas Jalcomulco
produce very heterogeneous landscapes in which and Rancho Real Minero (RRh4) are located
natural communities are fragmented but do not (19'1 9'39"-19'26'39"N, 96"44'08"-96'35' 18"W)
disappear completely. These landscapes provide a 20 km apart in the lower foothills of central Ve-
challenge to biodiversity studies, because at inter- racruz (Fig. 1). The original vegetation of both ar-
mediate levels of disturbance, diversity may actually eas was tropical deciduous forest (Castillo-Campos
increase (Connell 1975, 1978). 1995). Jalcomulco has a remnant of original veg-
In this paper, we examine how biodiversity re- etation with patches of different successionalstages.
sponds to habitat fragmentation at the local and The patch we studied (which covers ca 500 ha) was
landscape levels using dung beetles (Coleoptera: on a southward-facing slope and had an average
Scarabaeidae: Scarabaeinae) as an indicator group density of 12 trees and 8 shrubs per 100 m2. There
(Forsyth et al. 1998 and references therein; Halfier were no cattle on this slope, although cattle were
1998). We studied dung beetle communities in two present in small numbers in the flat valley bottom.
areas of central Veracruz that were once covered RRh4 measures 300 ha and contains patches of for-
est with an average density of 5 trees and 15 shrubs
continuously by tropical deciduous forest and sub-
per 100 m2 interspersed with pastureland contain-
jected to different types of human disturbance. We
ing species introduced 28 years ago (e.g., Sorghum
compared them with each other and to other dung
halapame and Cynodon plectostachyus). O n average,
beetle communities in central Veracruz.
40 head of cattle fed on a rotational basis in the
Veracruz is one of three states in Mexico that
pasture as well as in the forest patches.
have extremely high biodiversity (a megadiverse
area); however, it is also a region with one of the
SAMPLING METHoDs.-Four different trap types
highest amounts of habitat destruction. Contrary
were used to sample beetles. (1) The surface excre-
to what might be expected, and partly due to the
ment trap consisted of a 1-liter plastic container
complex orography of central Veracruz (with a gra- buried in the soil so that its rim was at ground
dient of 0 to 4250 m elev. over 80 km), the land- level. Each trap contained 150 g of fresh cow ma-
scape has not been affected in a uniform way by nure placed in a nylon stocking in the upper part
human activities as would have occurred if the land of the container, and the bottom of the container
were flat. The main consequence has been that was filled with 250 ml of water containing deter-
habitats persist as patches in the least accessible ar- gent. We placed 40 traps in each study area for a
eas and the landscape is extremely heterogeneous. 24-hour interval and 168 for periods of 12 hours
These patches, some of them quite extensive, have in order to distinguish between diurnal (0600-
been influenced by human activities to varying de- 1800 h) and nocturnal (1800-0600 h) activities.
grees, making Veracruz an appropriate location to (2) The surface carrion trap was constructed from
study the effects of fragmentation on biological di- a container similar to the preceding trap but was
versity. baited with 150 g of squid meat. The number of
Our working hypothesis was that the amount traps and the sampling periods were the same as
and quality of the food supply is the main factor with the previous traps. (3) The bottom excrement,
determining species richness and trophic structure or bottom carrion trap, was baited with 150 g of
in dung beetle communities. To test this hypoth- human excrement or 150 g of squid but was placed
esis, we compared one area with and one without on a layer of soil in the bottom of the plastic con-
cattle (large human-induced change in food sup- tainer. In this case, 20 traps of each type were left
ply), other environmental conditions being similar. for a 24-hour period. (4) The permanent necrotrap
We expected to find a large difference in the species (NTP 80; Mor6n & Terr6n 1984), which was de-
composition and rrophic structure of the two areas. signed to remain functional for long periods, had
We did not expect to find significant differences in bait consisting of 150 g of squid meat and was left
necrophagous beetles; among coprophagous bee- it in the field for 30 days. There were four traps
tles, we expected the area with cattle to have a per study area. We protected the first three types
much larger number of species, higher abundances from rain by covering them with a plastic plate at
146 Halffter and Arellano
FIGURE 1. Location of the study areas. Beetles represent sampling sites; arabic numbers: points of comparison used
in Table 2.
10 cm height from the rim of the trap. Finally, and uals was significantly different in relation to light
as a complementary method, we placed on two intensity (t = 132, P = 0.044).
(RRM) and three Ualcomulco) days in July 1996, To determine the degree of completeness of our
two baits of human excrement and two of squid samples, we calculated species accumulation curves
on a sheet of paper; in each, we counted the num- using the logarithmic and exponential or linear de-
ber of dung beetle individuals arriving on an hourly pendence models of Soberh and Llorente (1993),
basis. All captures were made in the rainy season and estimated the true species richness of each
(June-October) of 1994, 1995, and 1996, when study area using the s o h a r e SIGMA-STAT 2.0
numbers of species and individuals were highest. Uandel Corporation 1995; Fig. 2). The species ac-
We carried out two independent experiments cumulation curves accounted for 96.5 and 97.2
to account for the effect of light and that of cattle percent of the variance in sampling performance at
on the amount of dung beetles captured. To test RRM (P< 0.001) and estimated that we collected
for the effect of light, we laid out ten cow pats 87.5 and 95 percent of the true species richness
under the shade and ten cow pats under direct solar (Fig. 2a). For Jalcomulco, the models explained
radiation. To test for the effect of cattle presence, 90.8 and 96.1 percent of the variance (P< 0.001)
we laid out ten cow pats in each of two sites, one and estimated that we collected 100 and 105 per-
with and the other without cattle. We found no cent of the true species richness (the latter obvi-
significant differences in the amount of captured ously an error of the model; Fig. 2b). Additional
specimens in relation to cattle presence (t = 137.0, species of dung beetles are found in the flat agri-
P = 0.51 l ) , but the number of captured individ- cultural lands near our Jalcomulco study area; how-
Dung Beetles and Tropical Deforestation 147
TABLE 1 . Comparison of the abundance and biomass of dung beetle species in the two study areas.
mulco (N2 = 2.18): D. gi66osum (65.52%) and C. dominant species, both in terms of frequency and
cyanellus (13.26%); two also dominated in RFW in terms of biomass, were all rollers.
(N2 = 1.67): D. lo6ipes (76.37%) and Deltochilum With respect to ecological structure, Jalcomul-
sca6riusculurn (8.77%). In the former, the domi- co had a larger proportion of forest species and
nant species accounted for 78.78 percent of the non-digging species (Fig. 4). These differences,
total biomass and in the latter, 85.14 percent. The however, were not statistically significant (number
of forest-restricted species: x2 = 0.4505, P =
0.5938; biomass: t = 41.5, P = 0.165; frequency:
TABLE 2. Comparison of diversity measures obtained in t = 44.5, P = 0.318; Fig. 4a). In RFW,57.14
the two study areas. percent of the species were diggers, and in Jalco-
mulco, only 40 percent were diggers (Fig. 4b);
Real however, the difference between diggers and rollers
Jalcomulco Minero was not significant (number of species: x2 =
Based on abundances 0.4505, P = 0.5814; frequencies: t = 90, P =
NO 15.000 14.000 0.273; biomass: t = 86.5, P = 0.174).
Rl 1.950 1.691 With respect to feeding preferences, in Jalco-
R2 0.414 0.299 mulco 46.66 percent of the species were coproph-
H' 1.726 1.496
X 0.25 1 0.323
Nl 5.618 4.647
N2 3.986 3.097
E5 0.647 0.605
Based on biomass
NO 15.000 14.000
R1 1.266 1.016
R2 0.594 0.233 0 1
H' 1.249 0.912 0 I 2 3 4 5 6 7 8 9 1011IZ13
z:
20
0
cies of necrophagous beetles in Jalcomulco and four
in RRM,and there were no significant differences
between their frequency ( t = 36.5, P = 0.699) or
biomass ( t = 37.0, P = 0.818).
0Non-roller W Roller We found the three size categories to be equally
represented in Jalcomulco (33.33%) but there was
4 a higher percent of large species in RRM (42.86%;
%l-m
20
0
W Coprophagous
Fig. 4d). In Jalcomulco, we found only one species
of large, digging coprophages, Dichotomius ampli-
collis (1.5%); in RRM,there were two, D . ampli-
collis (4.08%) and Phanaeus tridenz (1.055%), the
two adding up to 5.13 percent of the total. There
was a larger number of diurnal species in Jalco-
0 Necrophagous mulco, whereas there was a similar proportion of
0Generalist nocturnal and diurnal species in RRM (Fig. 4e).
60 We expected to find greater biomass and a low-
er number of species in RRM. The total biomass
in Jalcomulco was 63,712.57 mg and in RRM,
359,782.9 mg, with 83.61 percent of the biomass
accounted for by only three species. In terms of
capture frequencies, we found greater equitability
W Large 0 Medium 0Small in Jalcomulco (Table 2). The following estimates
I00 of equitability (in terms of biomass) were derived
from the jackknife analysis: Jalcornulco = 0.6567
0
ml , ,
and RRM = 0.7154, with no significant differenc-
es between them ( K = 238.0, P = 0.228).
In contrast to the previous tests, in which we
did not find significant differences between the
study areas, Kendall's coefficient of concordance
among the ten most abundant species shared by
W Nocturnal 0Diurnal the study areas revealed significant differences
(Kendall's W = 0.0031, P = 0.049). Analysis of
the residuals of the contingency table revealed that
Uroxys boneti, C. cyanellus, Canthon (Ghphyro-
canthon) @moralis, D . gibbosum, D. lobipes, and D.
scabriusculum were significantly associated with for-
Jalcomulco RRM est patches and that Onthophap hoepfieri, D. am-
plicollis, and C. (G.) leech' were associated with
Study areas open areas containing cattle manure.
FIGURE 4. Structure of the Scarabaeinae group in the The cow pats monitored in 1996 attracted 49
two study areas: (a) spatial segregation; (b) food reloca- individuals of six species (including the three non-
tion; (c) segregation by food source; (d) segregation by forest species in the above table) in the open areas
size; and (e) temporal segregation. and only 3 individuals of two species under tree
cover. In Table 3, we compare these results with six
additional areas in central Veracruz that were orig-
agous, 33.33 percent were necrophagous, and 20 inally covered with tropical deciduous forest. We
percent were generalists. In RRM,50 percent of conclude from this comparison that, on one hand,
the species were coprophagous, 28.57 percent were a larger number of open area species is associated
necrophagous, and 21.43 percent were generalists with cattle, especially when most or all of tree cover
(Fig. 4c). We had hypothesized that the increased has been removed. O n the other hand, there is a
150 Halffler and Arellano
vU
,
DISCUSSION
Both the qualitative and quantitative analyses re-
vealed that there were more similarities than dif-
ferences in the diversities and guild structure of
dung beetles in Jalcomulco and RRM.The persis-
tence of tropical deciduous forest in both was more
important than the considerable difference in food
supply, consistent with the assertion of Halfier and
Matthews (1966) that tree cover was the most in-
fluential factor determining dung beetle commu-
nity composition in the tropics (particularly in the
New World). This leads us to speculate that most
of the dung beetles of the New World tropics
evolved in forests. Therefore, this group is an ideal
indicator of degree of forest destruction and mod-
ification.
Thirty species of dung beetles have been found
in the patchwork landscape of pastures and rem-
nant tropical deciduous and semi-deciduous forest
of central Veracruz (Table 4; see an analysis of bio-
geographic origin and composition in Halfier et
af. 1995). Point (alpha) diversities in central Vera-
cruz range between 8 and 18 (* = 11.5 ? 3.7;
Table 3). Jalcornulco with 15 species and RRM
with 14, are among the most species-rich patch-
work landscape areas. The number of species in
this landscape is much lower than the number in
the nearest tropical rain forest and associated com-
munities, Los Tuxtlas, which has 32 described
(Mor6n & Blackaller 1997) and at least 5 still un-
described species. The alpha number of species of
four tropical forests at Colombia (18-22 spp.; Es-
cobar 1997) is similar to the alpha value found at
the central Veracruz landscape. O n the other hand,
C Amazonia semu kzto landscapes have a much larger
.3
Y- 3 0 0 00000 number of species: 60 in Leticia, Colombia (How-
-g.3
W
nww
S N W
m o o ~ w
t-.m den & Nealis 1975); 54 in Ecuadoran landscape;
64 in VaupCs, Colombia; 74 in Tambopata, Perk
and 97 in Parque Nacional Noel Kempff Mercado,
Bolivia, with a maximum point (alpha) diversity of
64 species (Forsyth et af. 1998).
It is clear that species composition changes with
cattle presence in open areas, and more so if a sig-
nificant amount of the original tree cover has been
removed (Table 3): forest-restricted species give way
to heliophilous species as tree cover diminishes. O n
the other hand, the number of forest-restricted spe-
cies is larger where there has been less forest de-
Dung Beetles and Tropical Deforestation 151
species of dung beetles in forest and many in open Veracruz has probably had an extremely heteroge-
areas with livestock (cattle and sheep). neous and dynamic landscape of patches for at least
According to Kadiri et al. (1997), tree cover several hundred years. For an analysis on the evo-
acts as a filter to prevent invasion by most species lution of landscapes in Veracruz, see Guevara et al.
that live mainly in open areas, so that forests harbor (1997) and Guevara et al. (1998); for an analysis
an impoverished subset of open area species. Under on the development of cattle raising, see Barrera-
these conditions, increasing food availability in the Bassols (1992) and Skerritt (1992). This history
forest tends to cause rapid increases in the number explains two strange features of this study: the large
of individuals and total biomass and a slower in- number of native species in open areas and the
crease in the number of species. In contrast, in cen- survival of a large number of forest-restricted spe-
tral Veracruz and other parts of the New World cies in the landscape. Both situations lead us to an
tropics, the forest fauna and open-area fauna are interesting conclusion: as expected, a fragmented
distinct and the former is richer. Under these con- landscape has a partially different species compo-
ditions, an increase in food availability in the forest sition than the one of an unmodified tropical forest
will cause an increase in the number of individuals, landscape, but the fragmented landscape unit (not
but almost no change in species composition. Re- specific sites) has more species than the unmodified
duction in tree cover has the opposite effect of al- landscape. We show this for the Scarabaeinae, but
tering species composition. Thus, in the tropics it this may also be occurring with other organisms.
is tree cover and not food availability, as in France, To reach general conclusions, we need both to de-
that determines community composition (see com- velop more studies using different organisms and
ments on colonization of novel resources in pas- to take into account two considerations: the orig-
tures by tropical forest species in Hanski and Cam- inal vegetation type and the period of time since
befort 1991: 359). the beginning of the fragmentation process.
The major influence of human activities on Species of open areas are much more prevalent
dung beetle communities works through the effect in central Veracruz (where human-induced habitat
of these activities on the vegetative cover. These changes are very ancient) than in the large expanses
findings are consistent with the conclusion of Lob0 of tropical rain forest. Clearance of tropical rain
et al. (1998) that solar radiation is the most influ- forest has had a drastic effect because the com-
ential factor determining dung beetle activity. In munity of dung beetles then is made up almost
tropical regions formerly covered by forests, hu- exclusively of forest-restricted species (Howden &
man-induced changes influence dung beetles (and NeaIis 1975, Klein 1989). Even so, a few species
probably other taxa as well) by deleteriously affect- of open areas that did not occur previously in the
ing the survival of forest-restricted species and by forest interior have appeared in response to new
allowing forest invasion by native and introduced conditions (Halffter et al. 1992, Escobar & Medina
species of open areas. More forest-restricted species 1996, Escobar 1997). In central Veracruz, the dung
persist where more tree cover remains. There is a beetle communities of open areas are unsaturated,
gradient of decreasing richness of forest-restricted as revealed by the ease with which these commu-
species and increasing richness of open area species nities are invaded by species of open areas (e.g., D.
between Jalcomulco-Rancho Real Minero-Laguna gazella and E. intermediur, Montes de Oca &
Verde. An increase in food availability due to the Halffter 1998) as well as the rapid population in-
presence of livestock produces an increase in the crease in native species of open areas. In contrast,
number of individuals and biomass (the major dif- the communities of tropical forests in Veracruz, as
ference between Jalcomulco and RRM),but has a in the rest of the New World tropics, are saturated
small effect on species composition. (Hanski 1989).
Where fragmentation (as opposed to complete The abundance of three species of rolling ne-
destruction) of forest is as old as in central Vera- crophagous dung beetles, C. cyanellus and D. gib-
cruz, it is difficult to find an area in which we can bosum in Jalcomulco and C. cyanellus and D. lobipes
be sure that the habitat has not been disturbed by in RRM, is interesting (Table 1). Coprophanaeus
human activities. Complete forest clearance to de- Pluto, a digging necrophagous species, is character-
velop pastures for raising livestock is a 20th century istic of RRM. These abundances cannot be asso-
situation, but livestock raising arose in the 16th ciated with the presence of cattle. According to
century. Before the Spaniards arrived in Mexico, Hanski (1989: 489), tropical forests have a much
central Veracruz had a large human population that higher mammal species richness than temperate
performed slash-and-burn agriculture. Therefore, forests. Where there are more vertebrates, there will
Dung Beetles and Tropical Deforestation 153
be more carrion. O n the other hand, the abun- Portill0 read an early version of the manuscript and made
dance of small mammals (and their excrements) valuable suggestions. Dr. HCctor G 6 m a de Silva trans-
lated the original Spanish text into English. This study
the existence Of dung beet'es in forms part of the Parameters for Measuring Biodiversity
Jalcornulco (Table 1). and its Changes. Stage I. Ecological and Biogeographical
Analysis project (FB091/P168/94) and Parameters for
Measuring Biodiversity and its Changes. Stage 11. Devel-
ACKNOWLEDGMENTS opment of Examples project (FB532/K038/97) funded
We are grateful to Dr. Rogelio Macias for help with sta- by CONABIO. The second author acknowledges support
tistical analyses and Gonzalo Castillo for discussing the provided by a grant through the Theodore Roosevelt Me-
vegetation in the study areas. They and Dr. Jorge L6pa morial Fund.
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