Forest Ecology and Management 216 (2005) 117–133

www.elsevier.com/locate/foreco

Effects of deforestation on diversity, biomass and function of

dung beetles on the eastern slopes of the Peruvian Andes
Finbarr G. Horgan *
Population Ecology Group, Department of Biology, University of New Brunswick,
Fredericton, NB, Canada E3B 6C2

Received 21 March 2005; received in revised form 19 May 2005; accepted 20 May 2005

Abstract

Dung beetles play a major role in nutrient cycling in the tropics. While a number of studies have indicated decreasing
diversity of dung beetles as a result of deforestation, scant information exists on the implications of this for decomposition. This
study compares dung beetle assemblages at forest and deforested sites on the eastern slopes of the Peruvian Andes and examines
the importance of species richness and assemblage biomass in the decomposition of standardized dung pats. Results from pitfall
trapping indicated that species richness, assemblage biomass and the number of beetles arriving at dung pats were greater at
forest sites than at deforested sites. Although dung removal was generally faster at forest sites, between 50 and 100% of each
100 ml pat was removed within 3 days at all sites. Dung remained attractive to beetles for longer at forest sites, where it remained
moister, than at the deforested sites. Dung beetle activity significantly reduced the number of flies emerging from dung. In
an observation of decomposition of 96 separate dung pats, dung disappearance after 24 h was more frequently and more closely
related to total assemblage biomass than to species richness. This study indicates that deforestation results in a reduced
efficiency in decomposition by dung beetles that can be attributed mainly to reduced assemblage biomass at individual
dung pats.
# 2005 Elsevier B.V. All rights reserved.

Keywords: Biomass; Deforestation; Diversity; Dung beetles; Ecosystem function; Habitat change; Scarabaeidae

1. Introduction 1998). Recently, attempts have been made to convince

politicians, developers and the general public of the
It is clear that tropical deforestation is responsible ecological consequences of declining diversity in
for diversity loss across a range of taxonomic groups terms of material value systems where ecosystem
(Laurance and Bierregaard Jr, 1997; Didham et al., services are portrayed as being lost to humanity
(Ehrlich and Wilson, 1991; Naeem et al., 1994). There
has also been a call for a more direct, functional
* Present address: Teagasc, Oak Park Research Centre, Carlow,
Co. Carlow, Ireland.
approach to research on habitat change (Didham et al.,
Tel.: +353 59 9170237. 1996; Didham, 1998). However, for a number of
E-mail address: [email protected]. reasons, it has proved difficult to directly attribute

0378-1127/$ – see front matter # 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.foreco.2005.05.049
118 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133

losses in diversity to changes in ecosystem functions the edge of continuous forest often practice ‘slash-and-
(Huston, 1997; Schlapfer and Schmid, 1999; Rosen- burn’ agriculture (Rudel and Roper, 1997) leading to
feld, 2002; Ostfeld and LoGiudice, 2003). Further- non-equilibrium habitat with poorly understood con-
more, there is continuing uncertainty regarding how sequences for diversity.
experimental results scale up to landscape and The present study, conducted on the eastern slopes
regional levels or generalize across ecosystems and of the Peruvian Andes, compares dung beetle diversity
processes (Schlapfer et al., 1999; Loreau et al., 2001, and biomass in native forest and deforested agricul-
2002). Decreasing diversity is only one aspect of tural areas, and relates biomass and assemblage
habitat change; frequently associated with this are structure to two beetle functions: the burial of
shifts in biomass partitioning among functional groups omnivore dung and competition with dung breeding
and changes in the relative abundances of species flies. Dung burial is the initial step to most of the
(Jennersten, 1988; Didham et al., 1998). Despite the beneficial functions of tropical dung beetles and has
fact that ‘abundance’ is conceptually more compre- been related to the body mass of species in laboratory
hensible than ‘diversity’, studies that relate changes in studies (Doube et al., 1988; Doube, 1990; Horgan,
animal densities to ecosystem functions are still very 2001). The burial of dung by beetles and, therefore, the
rare (but see Jennersten, 1988; Bolam et al., 2002; removal of resources for competitors is also a
Niyogi et al., 2002). Recording losses in the mechanism by which dung breeding fly numbers
abundance of clearly beneficial taxa, as well as their may be reduced (Ridsdill-Smith et al., 1987). Few
diversity, could greatly contribute to conservation comparative field studies from the Neotropics have
education and influence policy makers when it is recorded decomposition, and those that have (i.e.,
linked to observed changes in easily understood Klein, 1989; Andresen, 2003) do not directly relate
ecosystem functions. decomposition to either dung beetle biomass or
One highly documented case of tropical diversity species richness. Furthermore, there are no compara-
loss that is linked to ecosystem function is the decline of tive studies on the effects of tropical dung beetles in
Neotropical dung beetles as a result of forest clearing reducing fly numbers in natural and disturbed habitats.
(Howden and Nealis, 1975; Klein, 1989; Kirk, 1992; The present study distinguishes between the roles of
Estrada et al., 1998). Tropical dung beetles offer a biomass and species richness in decomposition and
variety of clear ecosystem functions: they prevent soil- examines the influence of dung beetles on fly breeding
surface fouling by burying dung (Myrcha and from dung pats. It is one of only a handful of studies to
Andrzejewska, 1984; Cambefort, 1986; Davis, 1996); relate any aspect of change in insect assemblages to
they aerate soils, improve water penetration and prevent some ecosystem function compared across native and
nutrient loss through tunnelling and burial activities derived habitats (for other examples see Didham et al.,
(Edwards and Aschenborn, 1987; Herrich and Lal, 1996).
1996); they bury seeds and improve seed germination
rates (Shepherd and Chapman, 1998; Andresen, 2002,
2003) and they reduce populations of flies and other 2. Materials and methods
nuisance organisms (Fincher, 1975; Ridsdill-Smith
et al., 1987). During the last 50 years, huge tracts of 2.1. Study sites
native Neotropical forests have been cleared for timber
extraction or for agriculture (Riitters et al., 2000), which Experiments were carried out near San Ramón in
negatively affects local dung beetle assemblages the Department of Junı́n, Central Peru (Fig. 1). This
(Howden and Nealis, 1975; Klein, 1989; Estrada region, on the eastern Andean flanks, was originally
et al., 1998). In the lowland tropics, much of the covered with dense tropical premontane wet and rain
deforestation has been directed towards expanding forests (Holdridge classification in Stone (1992)). The
rangeland for cattle production (Flores Rodas, 1976; region is rich in vegetation and fauna (Tosi, 1960;
Rudel and Roper, 1997), whereas in many montane Emmons, 1997). Over the last 100 years, the area
regions, forests are traditionally converted to coffee or around San Ramón has been heavily exploited for
tree-crop plantations (Stone, 1992). Frontier farmers at shrub cultivation of coffee (Coffea spp.) as well as
 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133 119

Fig. 1. Map of study sites near San Ramón (shaded area at centre) and La Merced (shaded area to north). Heavy lines are rivers. Paired sites
include forest and forest fragments (open circles) and deforested/farm sites (open triangles) at 1, San Ramón; 2, Shimiyacu; 3, La Mosela; 4,
Signori; 5, Roman and 6, Gallegos. Inset map indicates location of the study area in Peru (solid square). Contours indicate altitude as metres
above sea level: two adjacent lines indicate a 200 m elevation change.

citrus (Citrus spp.) and banana (Musa spp.) produc- Sampling was mainly carried out at six locations
tion, and for timber logging (Stone, 1992). Recent with paired sites that included deforested areas (farms)
human immigration from the Andean highlands has with adjacent forest fragments or continuous forest
resulted in increased levels of ‘slash-and-burn’ (Fig. 1). Additional sites adjacent to La Mosela and
agriculture with the opening of ‘chacras’ or small- Shimiyacu were used in a series of decomposition
holding, subsistence farms that usually have a mix of experiments. Sites were chosen based on accessibility
crops including grains, cassava (Manihot esulenta during the rainy season, land-owner cooperation and the
Crantz) and bananas. The mean annual temperature is occurrence of adjacent forested and deforested areas
25 8C and annual precipitation is 2100 mm (data from with similar aspect. Because the sites were generally
the International Potato Centre weather station, San small, there were considerable differences between
Ramón at 820 m.a.s.l.). Temperatures at higher sites them in terms of topography, diversity and composition
(up to 1500 m.a.s.l.) were 1–2 8C lower and there were of crops and vegetation, and the degree of shade. The
substantially more rainfall hours each month at one CIP farm was generally open with no available shade,
pair of sites (sites at location 2 in Fig. 1) (unpublished whereas the Huaynarupay and La Mosela 2 farm sites
data). were shaded at certain times of the day due to local
120 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133

topography and adjacent tall-forest vegetation. Except within grids were separated by about 7 m. Pitfall traps,
for the CIP site, coffee bushes, bananas and cacoa which were plastic cups 10 cm deep with holes for
offered some shade at all sites: however, extensively draining water, were buried in the soil so that the mouth
shaded areas on the farms were avoided when setting- of the trap was flush with the soil surface. A tightly
out traps and experiments. Distances of from 1 to 15 km fitting funnel, 10 cm in diameter, was placed upright
separated each deforested site and each forest site. Part over the mouth of each cup. Baits of homogenized
of the forest at one site, Roman, was cut down in April human dung (25 ml) wrapped in muslin were placed
2002. Details of the sites are presented in Table 1. directly inside the traps. The traps were collected after
24 h. Most beetles were released after capture. At the
2.2. Study species Roman site, only 12 traps (2 grids) were used in
October–December because part of the forest had been
Many species of Scarabaeidae feed and reproduce cut down after the April–May sampling. To estimate
in mammalian dung. These can be separated into four species dry weight, the first 20 specimens (unknown
main groups based on their reproductive and nest sex) of each species captured were dried in a forced-
building behaviours (Doube et al., 1988; Doube, draught oven at 60 8C until a constant weight. Dry
1990). Ball rollers (telocoprids) form balls of dung, weights were used in estimating biomass. Further
which they roll some distance from the source pat. The details on the structure of dung beetle communities
dung is then buried in a superficial tunnel, or under from the forest and deforested sites will be addressed in
leaf litter, and a nest is constructed. Tunnellers a forthcoming paper. For the purpose of the present
(paracoprids) form tunnels directly beneath the source paper only species diversity and assemblage biomass
dung pat. The tunnels are then provisioned with dung (i.e., the total biomass of all dung beetles encountered at
and eggs are laid. Dwellers (endocoprids) do not a specific trap or bait) are considered.
relocate the dung but instead construct simple nests
within or beneath the dung pat. Some species oviposit 2.4. Biomass, species richness and dung removal
directly on the dung pat. A number of species use dung
that has been buried by others. These have been The relationship between assemblage biomass and
termed ‘‘kleptocoprids’’ (Doube et al., 1988; Doube, dung removal was examined at six forest sites in
1990). In the Neotropics the vast majority of dung October–December 2002. Pig dung was used in these
beetles are rollers or tunnellers (Gill, 1991). experiments because it was more readily available. Pig
dung and human dung are both highly attractive to
2.3. Beetle assemblages at forested and dung beetles. Preliminary studies indicated a similar
deforested sites richness and assemblage biomass of dung beetles at
pitfall traps baited with both types of dung (Wilk-
Pitfall trapping was conducted in 2002 to compare inson-rank (d.f. = 4): species richness, z =
0.37,
dung beetle assemblages in forested and deforested P = 0.71; biomass, z =
1.46, P = 0.14). Experimen-
sites. Trapping was conducted during only one night at tal pats (100 ml quantities of fresh pig dung) were
each site at the end of the rainy season in April and placed on the soil surface over mesh traps. Mesh traps
May (mean temperature 25.4 8C, mean daily rainfall were back-filled holes (ca. 15 cm deep  20 cm in
4.8 mm) and again at the onset of the following rainy diameter) lined with insect screening. Following
season between October and December (mean colonisation, tunneling beetles were retrieved by
temperature 26.0 8C, mean daily rainfall 7.6 mm). sifting through the soil held within the mesh (Doube
Dung beetle activity is often highest at the beginning and Giller, 1990). At each site, 16 traps were set out in
of the rains and drops off towards the end of the rainy a 4  4 configuration with each trap separated by
season (Gill, 1991). about 1.5 m. Traps were baited at about 16:00 h and
Thirty traps were set out at each site during each were collected 24 h later. The amount of dung
trapping period. The traps were arranged in 5 groups of remaining after 24 h of beetle activity was estimated
6 traps each (henceforth referred to as trapping ‘grids’). by collecting and lightly compacting surface remains
The grids were separated by 50–100 m while traps into graduated containers. Dung relocation estimated
Table 1
Paired forest–deforested sites near San Ramón where experiments were carried out during 2002–2004
Sites (number) a Latitude Longitude Altitude Slope Soil typeb Area Distance to Habitat description
(S) (W) (m.a.s.l.) (8) (ha) c edge (m)d
San Ramón (1)
El Tirol Nature Reserve 11808.20 75820.10 1000 40–80 Red-clays, shale 400 200–400 Old second-growth forest reserve
International Potato Centre 11807.60 75821.40 800 0–10 Sandy-loam 40 5000 Experimental farm with sweet-potato
(Hipomea batata) and pasture
Shimiyacu (2)
Upper Shimiyacu forest 11810.10 75818.20 1500 50–80 Red and 60000 3000 Continuous intact forest, adjacent to
grey clays Pui Pui Forest Reserve

F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133

Huaynarupay forest patch e 11810.50 75818.80 1300 10–20 Clays 1 20 Small forest patch on stony ground beside a mountain stream
Huaynarupay smallholding 11810.50 75818.80 1300 30 Clays 1.5 20 Recently cleared chacra (ca. 1–6 years) with banana, yucca,
paw paw (Carica papaya), corn (Zea mays) and potatoes
(Solanum tuberosum)
La Mosela (3)
La Mosela forest 1 11804.70 75822.90 1200 30–60 Sandy-loam 20 100 Catchment of Siete Casas Brook; old-growth forest patch,
surrounded predominantly by shade coffee
La Mosela forest 2e – – 1300 40–60 Clay-loam 2 25 Secondary forest and overgrown coffee bushes
La Mosela farm 1 11804.80 75822.90 1300 30–80 Clay-loam 0.5 20 Chacra recently cleared of 6-year-old secondary forest
(ca. 2 years) with banana, corn and beans (Fabia spp.)
La Mosela farm 2e – – 1200 10–20 Sandy-loam 0.3 10 Plot recently cleared of old coffee bushes and replanted
with smaller bushes. Generally open
La Perla (4)
Signori forest 11803.90 75822.00 1300 50–80 Deep-loam, 5 100–200 Regenerated forest on abandoned coffee plantation
some clay surrounded by shade coffee and tall brush
Signori farm 11804.80 75822.90 1300 0–40 Deep-loam 3 100 Farm dedicated to banana cultivation (>40 years)
Alta Cajacuri I (5)
Roman forest 11805.40 75824.20 1300 60–80 Sandy-loam-rocky 1000 50 Edge of continuous, largely-intact forest
Roman smallholding 11804.70 75824.40 1200 50 Sandy-loam 1 50 Recently cleared chacra (ca. 1-4 years) with
banana, yucca and avocado
Alta Cajacuri II (6)
Gallegos forest 11804.70 75824.40 1200 60 Sandy-loam-rocky 1 20 Forest patch, some selective logging. Connected
to continuous forest at higher altitudes by a narrow belt
of native vegetation, avocado and shade coffee
Gallegos smallholding 11805.40 75824.20 1300 80 Sandy-loam-rocky 0.5 50 Recently cleared chacra (ca. 1–4 years) with
corn and bananas
a
Numbers refer to locations indicated in Fig. 1.
b
Determined visually from soil pits.
c
Estimated area of habitat patch, connectivity to further patches of similar habitat is unknown for large forested areas.
d
Estimated distance between traps and the nearest contrasting habitat patch.

121
e
Sites used only in the comparative decomposition study.
122 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133

by this method correlates well with estimates using beetle-exclusion) was collected each day for 3 days.
dry weights of remaining dung (Pearson correlation: The baits were placed on dry sand in individual 1 l
r = 0.97, d.f. = 30, P < 0.001), but only for shaded plastic containers covered with muslin and held for 6
habitat such as forests. weeks in an insectary to allow flies to emerge. Flies
were identified to morphospecies, dried at 60 8C for 1
2.5. Dung removal at forested and deforested sites week, weighed and counted.
In July 2003, traps were set out at five locations
Between November 2002 and May 2004, a series of including Roman, Gallegos, La Mosela (two sites) and
comparative experiments were conducted to examine Signori to estimate decomposition and compare beetle
beetle activity and decomposition in forest and and fly assemblages at forest and deforested sites. At
deforested sites. The experiments were replicated at each location, two mesh traps and two pitfall traps were
Shimiyacu (including adjacent sites at the Huaynar- set out in forest and deforested habitat on the same day
upay property), San Ramón and at two separate sites at (two traps in each habitat for a total of four traps per
La Mosela. At each site, 100 ml volumes of pig dung site). Traps were baited with 100 ml of pig dung. Pitfall
were set out over 30 mesh traps;15 in forested and 15 baits were wrapped in 2 mm insect screening and were
in deforested habitat. All 30 were located in forested suspended over trap funnels on bamboo stakes such that
habitat at Shimiyacu in November 2002. Traps were they were ca. 2 cm over the traps. The traps were left for
separated by ca. 10 m. Ten pitfall traps baited with 2 days after which time they were collected and
100 ml of pig dung suspended ca. 2 cm over the funnel captures were recorded. Dung from the mesh traps was
on a bamboo stake, were also set out at each site (five lightly compacted into graduated containers, weighed
per habitat). Each day for 3 days, pitfall captures were and a 15 ml subsample was dried to estimate dung
recorded and 5 mesh traps were destructively sampled removal at each site. All the baits (including pitfall and
at each site. Pitfall traps indicated changes in the mesh trap baits) were then placed on dry sand in
attractiveness of dung over the 3-day period while individual 1 l plastic containers covered with muslin.
mesh traps indicated the presence of tunnellers and Containers were held for 6 weeks in an insectary to
dwellers at the dung pat (i.e., colonisation). Dung allow flies to emerge, after which time the baits were
removal was estimated by drying dung that remained dissected to remove all remaining fly larvae and pupae.
on the surface of the mesh traps at 60 8C until a Flies were identified to morphospecies, dried at 60 8C
constant weight and relating this to moisture estimates for 1 week, weighed and counted.
for the original dung, which was obtained from a
subsample of dung previous to setting it out in the 2.7. Data analyses
field. This method of estimating dung removal was
used here because the volume of dung remaining (as Dung beetle assemblage composition across sites
used above) is not a good indicator of dung removal in was examined using hierarchical cluster analysis. Data
open habitat where dung often dries quickly. for both trapping periods were combined for each site
and only presence/absence data were considered
2.6. Dung beetle and fly activity because beetle abundance can fluctuate considerably
over short time periods. Clusters were based on
At the same time as the July 2003 experiments calculated euclidian distances between sites.
described above, fly abundance and species richness The effects of habitat on the numbers of
were monitored using 100 ml baits of pig dung at forest individuals, beetle biomass, proportion of empty traps
and deforested sites (Huaynarupay and San Ramón sites and numbers of species per trapping grid were
only). Six baits were set out at each site, three of the analysed using paired t-tests. A split-block ANOVA
baits were wrapped in 2 mm insect screening that indicated that trapping period (early or late rains) had
excluded dung beetles but allowed flies to lay eggs into no effect on these parameters, therefore, samples from
the dung, a further three baits were open (unprotected both periods were pooled. Biomass and beetle
from beetles). Baits were randomly placed on the soil numbers were log (x + 0.1) transformed, proportions
surface at each site and one of each bait type (open and were arcsine-transformed and species numbers were
 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133 123

square-root transformed based on the distribution of

data. Following analyses, residuals were plotted and
found to be homogenous and normally distributed.
Linear regression was used to analyse decomposi-
tion rates at different sites. Species richness and beetle
biomass recorded from mesh traps were regressed
against dung removal during 24 h at forest sites (it is
assumed that ball rollers because of their generally
small size and low abundance, removed relatively
small amounts of dung compared to tunnellers).
Where residuals were not homogeneous despite
transformations, Spearman rank correlations were
used. Multiple regression with backward elimination
was used to examine the relative effects of biomass
and species richness on decomposition. Fig. 2. Cluster-diagram based on average linkage between dung
Temporal changes in dung remaining, dung water beetle species sampled in forest and deforested habitats at six
locations near San Ramón. Sites are separated into two main groups
content and beetle colonisation in the experiments
(I and II) based on species presence/absence.
conducted between November 2002 and May 2004
were analysed using GLM Analysis of covariance with
dung age as a repeated/split factor, and site and date as and Aphodiinae) (Appendix A). Voucher specimens
covariates. The GLM ANCOVA model was as have been deposited at the Museo de Historia Natural
follows: y = mean + dung age (repeated measure) + in Lima and at the Department of Entomology,
habitat + site + date + interactions. The GLM model Universidad Agraria La Molina, Lima. The author can
adjusts for interactions between covariates and the main be contacted for further details on voucher specimens
factors. Data residuals were checked for homogeneity and species identification.
and normality and transformed accordingly. Cluster analysis indicated two main groups of
The effects of trap-type and habitat on beetles and samples and two outliers (Fig. 2). Forest fragments
flies were analysed using a two-way ANOVA for data form a single cluster whereas the continuous forest at
collected in August 2003. Trap-type implies beetle Shimiyacu occurs as an outlying sample due to the
presence/absence in comparisons of fly parameters. relatively large number of species unique to the site
Dung remaining in deforested and forest habitat after (seven species). All deforested sites that were relatively
2 days was compared using a paired t-test. Repeated- close to forests or forest fragments formed a single
measure ANOVA was used to examine the effects cluster, whereas the deforested site at San Ramón occurs
of beetle exclusion from baits on fly colonisation in as an outlier due to the absence of most forest species at
July 2003. Results from both habitat types were the site (species are considered of the forest when >70%
pooled since habitat had no significant effect on of captured individuals occurred in forested habitat, see
fly-parameters in the experiment. Appendix A). Small numbers of forest species were
occasionally captured at all other deforested sites.
Species richness (forests = 8.80  0.95, deforested
3. Results = 4.57  0.79 (mean number of species per grid per
day  S.E.), t5 = 2.73, P = 0.041), number of indivi-
3.1. Beetle assemblages at forested and duals (forests 44.10  8.20, deforested = 15.13  3.85
deforested sites (mean number per grid per day  S.E.), t5 = 2.82,
P = 0.037) and total beetle biomass (forests = 3.69 
A total of 6393 beetles representing 52 species 0.71, deforested = 1.28  0.39 (mean gram dry weight
were captured throughout the study. Pitfall traps used per grid per day  S.E.), t5 = 2.50, P = 0.055) were
to compare assemblages captured a total of 3484 significantly greater at forest sites than at deforested
beetles from 47 species (excluding the Hybosoridae sites. The proportion of empty traps was generally
124 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133

Fig. 3. Relationship between the proportion of dung remaining after 24 h on the forest floor at six sites in October–November 2002 and: (A) the
number of species colonising each dung pat and (B) the biomass of beetles colonising each dung pat. Data are from La Mosela 1 (open circles),
La Mosela 2 (solid circles), San Ramón (open triangles), Roman (solid triangles), Gallegos (open squares) and Signori (solid squares).

higher in deforested habitat, but this was not statistically 5.1%, mean  S.E.) and beetle activity were low during
significant (forests = 0.10  0.03, deforested = 0.35  the experiment (Fig. 3). Unlike beetle biomass, species
0.10 (mean proportion  S.E.), t5 =
2.19, P = 0.080). richness was unrelated to dung disappearance at all sites
except at Roman, or when all sites were combined in a
3.2. Biomass, species richness and dung removal single analysis (Fig. 3; Table 2). Thus, although species
richness and beetle biomass in the traps were highly
The biomass of tunnelling beetles from mesh traps correlated (r = 0.86, d.f. = 95, P < 0.001), biomass
was positively related to dung disappearance after 24 h alone was a better predictor of decomposition (multiple
at five of six forest fragments (Fig. 3; Table 2). At the regression: y =
0.70x
0.36; r2 = 0.49, d.f. = 1.94,
remaining site, Signori, dung disappearance (17.3  P < 0.001) (Table 2).

Table 2
Summary of linear regressions and Spearman rank correlations evaluating the relationships between: (y) the proportion of dung removed from
each 100 ml bait at each of six sites near San Ramón and (x) total beetle biomass in each trap; and the relationship between (y) the proportion of
dung removed and (x) the number of species occurring in each trap
Site b a r r2 F P
Biomass
La Mosela 1a 0.81
0.0003 0.69 31.03 0.0001
La Mosela 2a 0.90
0.0003 0.66 21.54 0.0007
San Ramón 0.796 <0.001
Roman 0.917 <0.001
Gallegos 0.697 0.002
Signori 0.317 0.249
Sites combineda 0.96
0.0004 0.78 317.81 <0.0001
Species richness
La Mosela 1a 29.79 8.61 0.08 1.22 0.287
La Mosela 2a 48.47 6.77 0.04 0.44 0.521
San Ramón 0.136 0.709
Romana 112.94
14.41 0.45 9.15 0.012
Gallegosa 4.93 5.20 0.12 1.75 0.211
Signoria 6.19 5.98 0.04 0.52 0.485
Sites combined 0.62 <0.001
a
Equation of the form y = ax + b.
 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133 125

Fig. 4. Results of 10 repetitions of a decomposition experiment carried out for three successive days after fresh dung was placed in forest (open
circles) and deforested habitat (solid circles) near San Ramón, indicating: (A) the number of species captured in pitfall traps; (B) the total
biomass of beetles captured in pitfall traps; (C) the number of species captured in mesh traps; (D) the biomass of beetles captured in mesh traps;
(E) organic matter remaining at each pat and (F) dung water content. Bars indicate standard errors, n = 10 (rep 1), n = 5 (reps 2–10).

3.3. Dung removal at forest and deforested sites indicating that most beetles arrived shortly after fresh
dung was placed in pitfall traps. The results from
Beetle biomass and species richness generally pitfall traps indicate the richness and biomass of
decreased as dung aged (Fig. 4A and B; Table 3), beetles attracted to the baits and may include tourists

Table 3
F-values from covariance analyses of colonisation-decomposition parameters at San Ramón and Shimiyacu
Source of variation Pitfall traps Mesh traps Dung Rate of dung
No. of species Biomass No. of species Biomass removal dessication

Transformation sqrt log sqrt log arcsine arcsine

Error d.f. 95 95 92 79 83 77
Dung age 15.29*** 25.89*** 4.60* 3.65ns 28.82*** 11.08***
Site 0.69ns 4.42* 1.48ns 4.24* 0.24ns 65.32***
Date 5.30* 2.58ns 0.07ns 0.01ns 17.27*** 23.18***
Habitat 23.16*** 28.56*** 10.96*** 20.89*** 14.61*** 70.97***
Dung age  habitat 0.02ns 0.22ns 0.01ns 0.32ns 11.56*** 19.84***
ns, Not significant.
*
P < 0.05.
***
P < 0. 001.
126 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133

that do not utilize the resource. Mesh traps indicate

the species and biomass that remains at the dung
after initial colonisation. Both beetle biomass and
species richness were consistently higher in forest
than deforested sites, regardless of whether pitfall or
mesh traps were used (Fig. 4A–D; Table 3). In mesh
traps, species richness fluctuated, but beetle biomass
was generally constant over the 3 days (the Mosela
sites in July 2003 are notable exceptions) (Fig. 4C
and D; Table 3). Organic matter decreased over the 3
days at each site but the rate of dung removal varied
considerably across experimental replicates. Dung
became significantly dryer over the 3 days.
Desiccation rates varied between experimental
replicas, but drying was consistently and often
significantly faster in deforested habitat. Drying of
dung at La Mosela in both forest and deforested
habitat was generally slow (Fig. 4F; Table 3).
Significant dung age by habitat interaction effects on
the rates of dung removal and dung drying are
attributed to divergence in these rates at the end of
the 3 day experimental periods.

3.4. Beetle and fly activity Fig. 5. The effects of beetle exclusion on fly numbers, fly biomass
and the number of fly species emerging from 100 ml pig dung baits
The numbers and total biomass of flies emerging at four sites near San Ramón in July 2003 (means  S.E.). Baits
were collected after 1–3 days of exposure and held in containers
from baits were constant in the absence of dung until flies emerged. Solid bars indicate baits that were protected by
beetles, but declined where beetles had access to baits 2 mm plastic mesh, open bars are for unprotected baits that allowed
(Fig. 5). There was a significant interaction between access by dung beetles. Dung beetles actively removed dung from
bait type and day because fly abundance was similar in the unprotected baits over the 3-day period (ca. 26, 50 and 65% dung
both protected and open baits during the first day, but removal on days 1–3, respectively, see also Fig. 4).
was significantly reduced on the second and third days
(fly numbers: days, F 1,6 = 12.18, P = 0.013; presence/ was no significant interaction between the factors.
absence of beetles F 1,6 = 532.30, P < 0.001; interac- Species richness from mesh and pitfall traps was
tion F 1,6 = 12.52, P = 0.012. fly biomass: days, significantly related to dung removal across the sites
F 1,6 = 11.58, P = 0.014; presence/absence of beetles (pitfalls: y =
12.22x + 107.37, r2 = 0.51, P = 0.020;
F 1,6 = 42.50, P = 0.001; interaction F 1,6 = 13.22, mesh traps: y =
21.10x + 100.24, r2 = 0.64, P =
P = 0.011) (Fig. 5A and B). Fly species richness 0.006). Total beetle biomass in mesh traps was also
was also reduced by beetle activity (fly species related to dung removal (y = 0.06x + 90.03, r2 = 0.78,
richness: days, F 1,6 = 9.74, P = 0.210; presence/ P < 0.001). Biomass from pitfall traps was not related
absence of beetles F 1,6 = 18.08, P = 0.005; interaction to dung removal (y = 0.009x + 59.87, r2 = 0.05,
F 1,6 = 12.52, P = 0.012) (Fig. 5C). P = 0.54), largely due to a single outlying point with
In the August 2003 experiment, dung removal was high numbers of Canthon laesum, a medium-sized ball
significantly higher at forest than at deforested sites roller with a highly aggregated distribution. Signifi-
(Table 4). Habitat and trap-type did not influence the cantly more flies emerged from dung at deforested
biomass or number of beetles captured, but, more than at forest sites (Table 4). Fly densities were
species were captured in forested than in deforested approximately 6–8 times higher in pitfall than mesh
habitat, and in pitfall traps than in mesh traps. There traps (Table 4), indicating that dung removal and
 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133 127

Table 4
Biomass, abundance and species richness of dung beetles and flies at one forested and one nearby deforested site at each of five locations near San
Ramón during August 2003. The amount of dung remaining at mesh traps is also presented
Forest Deforested F-habitata F-trap-typea
Mesh Pitfall Mesh Pitfall
Dung Beetles
Biomass (milligram dry 957.17  197.60 1751.83  412.92 229.50  160.14 742.75  236.75 5.88* 4.85*
weight per trap)
Number of individuals per trap 16.33  4.72 30.17  6.57 6.25  1.55 12.50  4.95 5.89* 4.07
Number of species per trap 3.17  0.65 6.50  0.43 1.50  0.29 2.50  0.65 6.88* 9.91**
Flies
Biomass (milligram dry 0.003  0.002 0.111  0.003 0.008  0.004 0.110  0.003 0.99 1.01
weight per trap)
Number of individuals per trap 9.83  3.40 66.00  16.25 12.25  43.45 86.50  25.83 32.53*** 168.57***
Number of species per trap 1.50  0.34 1.33  0.21 2.25  0.75 1.50  0.65 5.53* 0.07
Dung remaining (%) 0.19  0.09 – 0.91  0.02 – 6.77**b
Two types of trap were used: pitfall traps prevented beetles from accessing the dung bait by trapping them in a buried pit, thereby allowing flies to
colonise and utilize the dung; mesh traps allowed both flies and beetles to colonise the dung. Numbers are means  S.E. (*P < 0.05, **P < 0.01,
***
P < 0.005). Summaries of two-way analyses of variance evaluating the effect of habitat (forest versus deforested) and trap-type on measured
parameters are also listed. Non-significant interaction terms were removed from models.
a
F-values, d.f. = 1,17.
b
Paired t-test, d.f. = 4, value presented is t.

burial by dung beetles reduced fly numbers associated forests. Dung removal by beetles also significantly
with dung in both habitat types. reduced the number of flies successfully breeding in
dung pats.
Few studies have directly linked diversity loss with
4. Discussion ecosystem functions. Changes in dung beetle assem-
blages due to deforestation and habitat fragmentation
4.1. General effects of deforestation have previously been related to reduced seed survival
and germination for some tropical plant species
According to this study, a dung pat on the floor of (Andresen, 2003) and reduced decomposition of dung
tropical forest on the eastern slopes of the Peruvian (Klein, 1989). However, evidence from the present
Andes generally attracts more beetles, of more study suggests that a reduction in numbers, and
species, than a similar pat in the deforested habitat therefore, total biomass of beetles attracted to dung,
typical of open farmland. Furthermore, dung may may have a greater effect on decomposition rates than
remain attractive to beetles for longer in forests than in does species loss.
deforested habitat because dung quality, indicated in Relating changes in the total biomass of beetles
these experiments by moisture content, is maintained that arrive at individual baits (assemblage biomass)
for longer under shade. This leads to quicker removal directly to deforestation is difficult because biomass
of dung in forest habitat by beetles that eventually is likely to be affected by resource availability
bury it as a food source or breeding substrate. The rate (Estrada et al., 1998; Cambefort and Walter, 1991).
of dung burial in forest habitat is related to both the Therefore, the differences observed in this study
total biomass and diversity of beetles attracted to the could simply be due to a lower amount of dung in the
dung. These two community parameters (diversity and more open deforested habitat. However, the trapping
biomass) are often confounded. However, biomass protocol used here is unlikely to have introduced an
alone explained a greater proportion of the variability excessive quantity of dung to the sites given that
in dung removal in the present study, suggesting a domestic (dogs, chickens and pigs) and wild
mechanism for faster decomposition of dung in (armadillo, agoutis and opposums) animals freely
128 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133

roamed the farms, and many beetles, including most 4.2. Deforestation and decomposition
of the open habitat species, are substrate generalists
that also feed on carrion, rotting eggs and dead As noted by Gittings et al. (1994), decomposition
invertebrates (personal observation). In fact, a experiments are simply snapshots of a dynamic
number of studies that compare tropical pastures, process. Decomposition will vary with soil hardness,
where dung is abundant, to forests, where it is rainfall, temperature and other abiotic factors (Davis,
frequently rare, indicate higher species richness and 1996; Herrich and Lal, 1996; Gittings et al., 1994). In
a higher abundance of beetles in the forests (Klein, the majority of experiments in the present study,
1989; Schiffler, 2003; Scheffler, 2005). Therefore, decomposition was faster in the forest. Notable
factors other than resource availability, such as exceptions included the very fast decomposition rates
increased levels of predation, competition with flies, at the deforested site at San Ramón in January 2003
or decreased searching efficiency, probably con- and at Huaynarupay in July 2003. In the former, rapid
tributed to the lower assemblage biomass in dung burial by Diabroctis mimas mimas (L.), a large
deforested habitat. (ca. 550 mg dry weight) diurnal species, and dung
The extent and rate of deforestation in Latin consumption by muscid flies were conspicuously high.
America have been so great that it is difficult to In the latter, another large diurnal species, Oxysternon
understand the degree to which current forest conspicullatum Weber (ca. 350 mg dry weight), was
assemblages reflect the changes, since for many common and buried large amounts of dung at each pat.
organisms, edge effects can extend well into the forest Differences in decomposition rates were never great,
interior (up to 10’s of km) (Didham, 1998; Didham since dung in both habitat types disappeared within 1
et al., 1998; Laurance et al., 2002). The present study week. However, dung remained consistently moister
was carried out in a mosaic of forest fragments and in the forest, where colonisation by beetles often
open farms now typical of the Andean foothills, where continued for longer, particularly in the July experi-
vegetation on relatively flat terrain is generally heavily ments. Horgan (2002) showed similar trends with
altered whereas steep slopes remain relatively well Salvadoran dung beetles and suggested that colonisa-
conserved (Stone, 1992; Medina et al., 2002). In this tion of dung in pastures occurred during a longer
study, the open habitat typically encountered at the period under shade than in the open because dung
deforested sites had a surprising diversity of species quality was maintained for a longer period in the
when compared to other studies from similar habitat shade.
and altitudes in the Andes (e.g., Medina et al., 2002; In spite of the preliminary nature of the fly-related
Escobar, 2004). However, beetle assemblages at all experiments, it is clear that beetles reduced fly
sites, in both deforested and forest habitat, were likely numbers emerging from the dung. While not
influenced by their proximity to edges. In spite of the examined, the principal mechanism probably involves
fragmented nature of the landscape, many species a reduction in resource availability for flies through the
were restricted to the forest. It appears that as farms active removal of dung by beetles. Large predatory
become increasingly distanced from forested areas (as staphylinid beetles were generally rare at the sites,
at CIP, San Ramón), generalist species begin to whereas smaller staphylinids were able to penetrate
disappear. For example, Oxysternon and Eurysternus the 2 mm mesh (personal observation). Dung beetles
species that occurred at some farm sites, were never cannot use hard, dry dung, and, where beetles are not
captured at CIP and were also absent from isolated involved in decomposition after 1–2 days, flies,
shaded habitats (a stand of teak-trees and a citrus already present in the dung at that time, may
grove) near the town of San Ramón (personal completely consume the remainder of the pat. This
observation). The relatively rich assemblages in forest was particularly apparent at the deforested site at San
fragments at La Mosela and Signori suggest that Ramón in January 2003 where pats contained
shade-coffee helps maintain diversity. Similar trends conspicuous masses of fly prepupae (Muscidae) by
have been noted in other forest-agriculture mosaics in the third day (personal observation). Higher tempera-
the Neotropics (Morón, 1987; Estrada et al., 1998; tures in open deforested habitat will increase the rates
Escobar, 2004). of fly development and may give flies an advantage
 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133 129

over dung beetles. Flies play a functional role in the Scottish mudflats but that these effects were mainly
ecosystem by breaking down dung. However, they do driven by the presence of the largest species in the
not construct tunnels or relocate dung and therefore system. The fact that beetle biomass was generally
play little or no role in pedoturbation or secondary more directly related to dung disappearance than was
seed dispersal. Also they are noted to cause ammonia species richness in this study should not be taken as
loss during decomposition when compared to dung evidence of functional redundancy. This study
beetles (Macqueen and Bierne, 1975). excluded natural variability from the experiments
by standardizing dung pats (i.e., one type of
4.3. Diversity-function or biomass-function? homogenized dung, one volume and shape, and
deposited at the same time each day). It is still
The question of whether species diversity affects unknown how species might respond functionally to
ecosystem functions has recently drawn consider- natural variability in resource patches (see Rosenfeld,
able attention. In a comprehensive review, Huston 2002).
(1997) indicates that there is a tendency to interpret The results obtained here agree with those of Klein
experimentally obtained non-linear relationships (1989) and Andresen (2003), both of whom addressed
between diversity and function as evidence for the functional role of dung beetles under varying
functional redundancy. This occurs despite a range degrees of habitat fragmentation in Amazonia. How-
of problems associated with diversity-function ever, it is difficult to separate the effects of biomass from
experiments, including difficulties in semantics species richness in these previous studies. A reanalysis
and theory, as well as protocols that often rely on of Andresen’s (2003) data (using her Figs. 1 and 2)
broad assumptions. Much less attention has been indicates strong relationships between dung removal
placed on biomass changes that result from habitat and both species richness (r2  0.98) and an index of
loss or the effects of biomass loss on ecosystem biomass (number of individuals  mean beetle size)
function (but see Bolam et al., 2002; Niyogi et al., (r2  0.57). In a reanalysis of Klein’s data, Didham
2002). et al. (1996) indicate that the decrease in the rate of
As noted by Bengtsson (1998), the effects of decomposition in small forest fragments may be due
biomass on ecological functions may be easier to more to a huge decrease in population densities of dung
examine than the effects of diversity, since diversity is beetles than to a small decline in species richness. In
an abstract property of the species in the context of Klein’s study, many typically large species (i.e.,
ecosystems and as such lacks direct, mechanistic Atuechus spp., Dichotomius spp. and the Phaenini)
relations to ecological functions. In contrast, biomass declined as patches became smaller. As suggested by
can be mechanistically related to ecological processes Didham et al. (1996), these forest species may have
through feeding, uptake and physiology (Bengtsson, become so rare as to be functionally extinct. Mean-
1998). If biomass is important, then larger species will while, the generally small Glaphyrocanthon spp.
have a greater influence on ecosystem functions. This dominated in clearcuts. Therefore, changes in total
draws attention to the shortcomings of using a biomass were more closely related to decomposition
unidimensional parameter, such as species richness rates than was abundance. Clearly, more emphasis
which incorporates possible idiosyncratic effects should be placed on the importance of biomass in future
(where species’ identity matters more than diversity). studies of ecosystem function.
For example, species richness and biomass were
similar in forest and deforested sites at Huaynarupay,
but dung removal was particularly fast at the 5. Conclusions
deforested site due to large numbers of O. con-
spicullatum, which buries large amounts of dung in There is an urgent need for further studies with a
just a few hours (personal observation). Similarly, functional approach that can emphasize the losses to
Bolam et al. (2002) have shown that changes in the society and the environment that result from certain
biomass and species richness of bentic macroinverte- types of landscape change (Didham et al., 1996). Data
brates had significant effects on O2 consumption in from studies that emphasize ecosystem functions will
130 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133

play a valuable role in education, even where direct Acknowledgements

causal relationships for decreased functions have not
yet been elucidated. The present study suggests a The author thanks H. Huaynarupay-Pienado, J.
mechanistic relationship between biomass and eco- Gallegos, C. Jordan, O. Baca, P. Roman, S. Signori, the
system function from field data. It demonstrates that International Potato Centre (CIP) and the municipality
deforestation reduces local dung beetle diversity and of San Ramón for access to field sites (Santiago Signori
abundance and that this is related to a reduced sadly died in 2004); B. Gill, F. Génier and H. Howden
efficiency in dung removal, a first step in decomposi- are thanked for identifying beetles; the Museo de
tion. Biomass and diversity will generally be Historia Natural (Lima, Peru) for holding voucher
confounded in field studies. Future experimental specimens; C. Torpoco for help with fieldwork and G.
diversity-function studies could avoid this problem Forbes, P. Giller, S. Heard, J. Loo, C. Lucarotti, C.
by maintaining a constant biomass while varying Paponnet-Cantat, Y. Pelletier, D. Quiring and anon-
species richness or diversity. Furthermore, experi- ymous reviewers for many helpful comments that
ments should pay increased attention to species improved the manuscript. This work was supported by
identity and to species-specific characteristics that Agriculture and Agrifood Canada (Y. Pelletier) and a
can be related to function. NSERC discovery grant (D. Quiring).

Appendix A
Beetles captured in different experiments at forest and deforested-farm sites in Chanchamayo, Peru.
Speciesa Number of beetles captured
Community Decomposition Comparative Flies Total
composition decomposition
Farm Forest Forest Farm Forest Farm Forest
Large tunnellers
Coprophanaeus t. telamon Erichson [3] 12 4 0 0 0 0 0 16
Diabroctis mimas mimas (L.) [4] 1 0 0 4 0 0 0 5
Dichotomius adrastis [13] 9 66 0 1 202 0 0 278
Dichotomius fissus (Harold) [14] 0 2 0 0 0 0 0 2
Dichotomius sp.1 [15] 80 360 148 52 185 3 22 850
Dichotomius sp.2 [16] 66 470 193 30 106 31 141 1037
Dichotomius sp.3 [54] 0 1 0 0 0 0 0 1
Ontherus alexis (Blanchard) [18] 64 168 12 0 97 0 1 326
Ontherus obliquus Génier [19] 0 0 0 0 31 0 0 31
Ontherus pubens Génier [20] 24 0 0 109 2 0 0 128
Oxysternon conspicullatum Weber [5] 1 4 4 38 19 1 1 68
Oxysternon smaragdinum Olsoufieff [6] 4 15 0 2 0 0 0 21
Phanaeus chalcomelas (Perty) [1] 2 182 12 1 69 1 6 273
Phanaeus meleagris Blanchard [2] 0 2 0 0 4 0 0 6
Small tunnellers
Ateuchus laevicollis [17] 0 78 2 0 3 0 0 83
Ateuchus sp.1 [45] 0 1 0 0 0 0 0 1
Ateuchus sp.2 [53] 0 17 0 0 1 0 0 18
Onthophagus gr. clypeatus [22] 36 33 23 11 29 1 14 147
Onthophagus haematopus [23] 3 16 3 2 0 0 0 24
Onthophagus sp.1 [24] 10 0 0 142 0 0 0 152
Onthophagus sp.2 [57] 0 1 3 0 0 0 0 4
Canthidium sp.1 [38] 10 263 95 4 100 0 0 472
Canthidium sp.2 [39] 45 0 0 5 0 0 0 50
Canthidium sp.3 [40] 0 3 0 0 0 0 0 3
Canthidium sp.4 [41] 0 9 0 0 6 0 0 15
 F.G. Horgan / Forest Ecology and Management 216 (2005) 117–133 131

Appendix A (Continued )
Speciesa Number of beetles captured
Community Decomposition Comparative Flies Total
composition decomposition
Farm Forest Forest Farm Forest Farm Forest
Canthidium sp.5 [42] 1 13 0 0 0 0 0 14
Canthidium sp.6 [43] 0 4 0 0 0 0 0 4
Canthidium sp.7 [na] 0 0 0 1 0 0 0 1
Uroxys sp.1 [52] 8 81 201 5 155 0 47 497
Large ball rollers
Deltochilum burmeisteri [10] 0 8 0 0 10 0 0 18
Deltochilum laevigatum [11] 8 22 0 0 16 0 0 46
Deltochilum orbiculare Lansberge [9] 0 3 0 0 1 0 0 4
Deltochilum sp.1 [51] 0 4 0 0 0 0 0 4
Streblopus punctatus [21] 0 1 0 0 0 0 0 1
Small ball rollers
Canthon laesum [28] 2 303 0 0 0 1 9 315
Canthon literatum [35] 100 0 0 31 0 8 0 139
Canthon luteicollis Erichson [29] 219 0 0 115 2 0 0 336
Canthon sublyalinus [32] 2 28 0 0 0 0 0 30
Canthon virens chalybaeus [33] 200 0 0 57 0 29 0 286
Canthon sp.1 [30] 12 5 0 0 0 0 0 17
Canthon sp.2 [34] 0 2 0 0 2 0 1 5
Canthon sp.3 [55] 1 8 0 0 1 0 0 10
Canthon sp.4 [56] 0 5 0 0 0 0 0 5
Pseudocanthon xanthurum (Blanchard) [50] 0 0 0 16 0 0 0 16
Scybalocanthon trimaculatus Schmidt [36] 0 44 0 0 9 0 1 54
Silvicanthon bridarollii [37] 0 122 0 0 24 0 6 152
Eurysternini dwellers
Eurysternus caribaeus (Herbst) [47] 12 63 4 1 61 0 9 150
Eurysternus velutinus Bates [46] 8 9 1 14 23 0 1 56
Eurysternus sp.1 [48] 1 140 0 0 23 0 20 184
Eurysternus sp.2 [49] 0 6 1 0 0 0 0 7
Eurysternus sp.3 [na] 0 0 0 0 1 0 0 1
Total individuals 941 2573 702 641 1182 75 279 6393
Total species 29 41 15 22 28 9 15 52
a
Numbers refer to numbered voucher specimens held at the Museo de Historia Natural and the Department of Entomology, Universidad
Agraria La Molina, Lima, Peru; na, no voucher specimen available.

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