The final publication is available at Springer via http://dx.doi.org

The final publication is available at Springer via http://dx.doi.org/10.1007/s10531-009-9643-1
Anna Lorenza Maria Macagno1, Claudia Palestrini1
The maintenance of extensively exploited pastures within the Alpine mountain belt: implications
for dung beetle conservation (Coleoptera: Scarabaeoidea)
1
Dipartimento di Biologia Animale e dell’Uomo, Università degli Studi di Torino, Via Accademia
Albertina 13, 10123 Torino, Italy
Email: [email protected]
Abstract
The abandonment of marginal areas and the decline of traditional small-scale cattle-breeding is
bringing about substantial changes in many areas of the Alpine mountain belt. Extensively
exploited pastures, which were colonized by typical ecological communities, are now being
replaced by shrublands and forests. In this paper, we evaluate the effectiveness of the
maintenance of small pastures for dung beetle (Scarabaeoidea: Geotrupidae, Aphodiidae,
Scarabaeidae) conservation in a protected area of the north-western Italian Alps. From July until
September 2007, we studied the dung beetle coenosis in the main habitats of the mountain belt:
beech forest, scots pine forest, mountain pine forest and pasture. Twenty-three species were
sampled. We compared abundance, species richness, α-diversity, evenness and species turnover
between the four habitat assemblages and performed a correspondence analysis based on
dominance patterns of the three families. Two main ensembles were identified: a pasture
ensemble, highly diverse and dominated by Scarabaeidae, and a closed habitats ensemble, less
structured and dominated by Aphodiidae and Geotrupidae. Combining habitat specificity and
fidelity, the IndVal method showed that half of the species collected made a strong habitat
selection toward pasture, while only C. granarius (Aphodiidae) was a reliable indicator of woody
areas. We therefore conclude that the loss of extensively exploited pastures may bring about
fundamental changes in dung insect communities. In protected areas, a management policy
intended to preserve the traditional, sustainable human activities within the mountain belt is
highly recommended for the conservation of these insects.
Keywords
Alps Conservation management policy Diversity Dominance pattern Evenness Habitat selection
IndVal Species turnover
Abbreviation
FAG
Beech (Fagus sylvatica L.) forest
PAS
Pasture
PS
Scots pine (Pinus sylvestris L.) forest
PU
Mountain pine (Pinus uncinata Mill. ex Mirb.) forest
Introduction
The impact of man has determined profound environmental modifications on the Alps. Six
thousand years ago, portions of pre-existing forests and shrublands began to be cleared or burnt to
increase the availability of open grasslands for livestock (Lichtenberger 1994). Pastoral activities
have been practised ever since, shaping the alpine landscape and increasing the ecomosaic
complexity below the timberline. Along with this gradual modification process, many plant and
animal species took advantage of newly established habitats such as extensively exploited
pastures, which were colonized by typical ecological communities (Wettstein and Schmid 1999;
Chauchard et al. 2007; Negro et al. 2007).
At the end of the nineteenth century, increasing industrialization gave rise to deep socio-economic
changes that caused the abandonment of marginal areas and the decline of traditional small-scale
agriculture, cattle-breeding and forest resource utilization. In Alpine regions, the ecological
consequences of this process are evident mostly below the timberline, where grasslands are
gradually turning into shrub and, eventually, forest. The abandonment of traditionally exploited
environments such as meadows and pastures is leading to an impoverishment of their typical
ecological communities (Laiolo et al. 2004): alpine biological diversity is therefore changing as a
consequence of land use dynamics (Farina 1991; Giupponi et al. 2006).
Coprophagous communities formed by lamellicorn beetles (Scarabaeoidea: Aphodiidae,
Scarabaeidae, Geotrupidae) play a key role in ecosystems, especially in agro-ecosystems. By
burrowing and decomposing animal wastes they actively participate in soil enrichment and
nutrient cycling as well as secondary seed dispersal and parasite suppression (Fincher 1981;
Martín-Piera and Lobo 1995; Nichols et al. 2008). Besides resource availability (Carpaneto et al.
2005), various environmental factors influence Scarabaeoidea distribution: soil type and moisture,
elevation, exposure and vegetation structure (Halffter and Matthews 1966; Doube 1987; RomeroAlcaraz and Ávila 2000; Kanda et al. 2005; Jay-Robert et al. 2008a). There is therefore increasing
interest in dung beetles as bioindicators of habitat transformation (e.g. McGeoch et al. 2002). It is
assumed that these communities have been structuring along with gradual, man-driven smallscale landscape modifications (Verdú et al. 2007). Sudden environmental changes have
nonetheless proven detrimental to them (Kanda et al. 2005). In Alpine regions, as in most of
Europe, Scarabaeoidea are likely to be particularly affected by the decline of traditional livestock
raising (Jay-Robert et al. 2008b). This process may bring about deep changes in dung beetle
communities (Borghesio et al. 2001) because it deprives them of food resources which used to be
supplied by domestic livestock in the past and force them to be increasingly dependent on usually
scarce wild mammal populations (Lumaret 1990; Biström et al. 1991; Jay-Robert et al. 2008b).
Over the past 20 years, there has been a strong debate on whether management and protection
policies of Alpine areas should aim to restore the wilderness by completely removing human
influences (Zunino 1980; Broggi 1995) or to protect and maintain traditional land mosaics that
include relicts of natural vegetation along with low-impact, sustainable land use (Höchtl et al.
2005). Mont Avic Natural Park (Aosta Valley, N–W Italian Alps), where the study presented in
this paper took place, chose the second type of management policy. In this protected area, organic
farming (Milestad and Hadatsch 2003) is supported and maintained by farm subsidies (Broglio
1996). The traditional landscape mosaic is maintained by means of low-impact grazing practices,
particularly within the mountain belt (i.e., areas between 1,000 and 1,500 m a. s. l., which
underwent a gradual landscape modification after the introduction of cattle-breeding, thanks to the
creation of open areas to be used as pastures).
The present study was conducted during the summer of 2007 and examined the coprophagous
entomofauna within the Mont Avic Natural Park mountain belt, with the aim of:
1. Providing a detailed analysis of the structure of dung beetle assemblages (Scarabaeoidea:
Geotrupidae, Aphodiidae, Scarabaeidae) living in the main habitats below the tree line, namely
beech forest, scots pine forest, mountain pine forest and pasture.
2. Highlighting patterns of habitat selection at both family and species level.
Combined, these approaches allowed us to assess the relative contribution of natural and
extensively exploited habitats (pasture) to overall dung-beetle diversity. Results therefore allowed
to test the effectiveness of the maintenance of small pastures, through the encouragement of
traditional small-scale livestock raising, for the conservation of these insects.
Materials and methods
Study area and sampling design
Mont Avic Natural Park (Aosta Valley, N–W Italian Alps: Fig. 1) was instituted in 1989 with the
aim of achieving biodiversity conservation by rationalizing the management of agro-pastoral
activities traditionally conducted in the area through a “sustainable development” approach
(Palestrini et al. 2007–2008). Today, the entire protected area encompasses 5,747 ha along an
altitudinal gradient that ranges from valley floors (~600 m a. s. l.) to 3,185 m a. s. l. Previous
studies on the coprophagous entomofauna of the Park and the adjacent areas of Val Chalamy
(Barbero et al. 1994; Palestrini et al. 2007–2008) involved faunistic surveys covering all
altitudinal zones: the hill belt (<900 m), the mountain belt (900–1,500 m), the subalpine belt
(1,500–2,200 m), the lower alpine belt (2,200–2,600 m) and the nival belt (>2,600 m).
The present study took place in the mountain belt of Val Chalamy. Four sampling sites where
identified within the main habitats below the tree line in the area: beech (Fagus sylvatica L.)
forest, scots pine (Pinus sylvestris L.) forest, mountain pine (Pinus uncinata Mill. ex Mirb.) forest
and pasture, hereafter referred to as FAG, PS, PU and PAS, respectively. A transect made of six
pitfall traps spaced 20 m apart and baited with 150 g fresh cow dung suspended in gauze (model
CSS in Lobo et al. 1988) was positioned at each site.
Based on findings about the effect of landscape matrix and vegetation openness on paleartic dung
beetle diversity (e.g. Lumaret and Kirk 1991; Roslin and Koivunen 2001; Numa et al. 2009), a
characterization of sampling sites was conducted by analyzing the vegetation structure within a
buffer of 100 m from the transects (Cremonese et al. 2007) (Fig. 1).
PS (Utm ED50 391373, 5059947). Located near La Voella, 1410 m a. s. l. on the south facing
slope of Val Chalamy, the site has a total plant cover of 70%. It is a dense scots pine forest with
associated undergrowth of Rhododendron ferrugineum L., Juniperus communis L. and Vaccinium
myrtillus L. covering approximately 60% of the soil beneath the trees.
PU (Utm ED50 390355, 5059453). Also on the south facing slope of Val Chalamy, near locality
Magazzino, the site is 1,502 m a. s. l. and is dominated by mountain pines, associated with rare
scots pines and hybrids. The total plant cover is of 60%. The undergrowth (of which
representative plants are Juniperus communis L., Arctostaphylos uva-ursi (L.) Spreng.,
Antennaria dioica (L.) Gaertn., Rhododendron ferrugineum L., Vaccinium sp. and Calluna
vulgaris (L.) Hull) covers 90% of the soil beneath the trees.
FAG (Utm ED50 394210, 5059329). The site is located near the village of Boden, 1,050 m a. s. l.
on the north facing slope of Val Chalamy. It is a beech forest with a total plant cover of 90% and
little to no undergrowth. Small associations of Betula pendula Roth, Corylus avellana L., Populus
tremula L. and Populus nigra L. are scattered within the main forest.
PAS (Utm ED50 394432, 5059224). Also on the north facing slope of Val Chalamy, the site is a
small herbaceous area (0.8 ha) located 1,002 m a. s. l. near the village of Gettaz. It was subjected
to 1-month-long grazing activity before sampling began and was never visited by cattle afterward.
The site is surrounded by patches of mixed broad-leaf woodland dominated by beech and other
small pastures that are regularly grazed by cattle at the beginning of the summer.
The minimum distance from two traps belonging to different transects was 250 m (PAS-FAG). To
evaluate differences between habitats, transects were carefully located in an east-facing position
to minimize the effect of exposure, which has recently proven highly effective in shaping dung
beetle community patterns (Jay-Robert et al. 2008a). The trapping period lasted from July 14th to
September 29th 2007. All traps were emptied and re-baited every week on the same day. Trapped
beetles were counted and identified to species level using standard keys (Martín-Piera and LópezColón 2000; Dellacasa and Dellacasa 2006).
Data analysis
A completeness analysis of sampling in each habitat studied was conducted by preliminarily
computing an abundance-based richness estimator (ACE) with EstimateS 8.0.0 (Colwell 2006),
and then measuring inventory completeness as the percentage of species observed from the total
number of species predicted by the estimator (Verdú et al. 2007).
Samples collected at each trap were characterized by computing parameters that included species
richness (S), abundance (A) and α-diversity (αDIV: Shannon–Wiener) indexes. Data were
normalized
log(αDIV + 1)] prior to analysis. Differences between habitats
were assessed holding habitat as fixed factor and controlling for phenology-induced variations by
fitting sample date as random factor in a two-way ANOVA. Least-squares deviation (LSD) posthoc tests were used for pair-wise habitat comparisons.
Two or more assemblages may have the same α-diversity values without necessarily having the
same species composition and evenness. The species turnover among habitats was therefore
quantified using the β-diversity Whittaker’s index (Magurran 2004): β w = (S/a)−1, where S is the
total number of species and a is the average number of species in compared assemblages.
Whittaker’s index varies between 0 (identical species composition) and 1 (completely different
species composition) (Whittaker 1960). Changes in evenness among habitats were first inspected
by plotting log-transformed abundances of beetles against species rank and then fitting to the
distributions the log-linear Motomura’s model (Motomura 1932): log(N) = a × R + b, where N is
the abundance of a collected species and R is the rank of the same species. Kolmogorov-Smirnov
tests on linear regression residuals were carried out to test for the adjustment of the model. The
higher the slope the more the assemblage is dominated by a single abundant species (Errouissi et
al. 2004; Magurran 2004): angular coefficients of regression lines can be therefore interpreted as
an evenness proxy. After testing for homoscedasticity with a Levene test (Levene 1960),
comparisons of angular coefficients between habitats where carried out by checking the
significance of interaction of log(N) and species rank with an ANCOVA (Engqvist 2005).
To highlight the dominance patterns in each habitat, beetles trapped on each sample day in the
same habitat were pooled and a Correspondence Analysis (CA) with the relative abundances of
subfamilies was carried out (Jay-Robert et al. 2008a). The IndVal (Indicator Value) method
(Dufrêne and Legendre 1997) was then used to assess characteristic species of the studied
habitats. The IndVal of a single species is expressed as the product of specificity and fidelity
measures. It reaches its maximum (=100) when all individuals of a species are found in a single
habitat type (high specificity) and occur at all pitfall traps in that habitat (high fidelity) (Dufrêne
and Legendre 1997). This approach generates a significant value for the strength of association by
using a randomized re-sampling technique (Monte Carlo randomization with 5000 permutations).
The IndVal method needs a preliminary classification of sample sites: in this case a dendrogram
was constructed on the basis of the abundance of each species per habitat by means of a
Euclidean-distance single-link hierarchical clustering. Statistical analyses were performed with
SPSS 13.0, STATISTICA 6.0 and Program IndVal v. 2.1 (Dufrêne 2004).
Results
A total of 4,538 beetles belonging to 23 species were caught during the study period (Table 1).
This accounted for 82% of the dung beetle species found in the entire protected area (Palestrini et
al. 2007–2008). Results of the completeness analysis of sampling showed that the sampling effort
was adequate in all habitats: our inventories were more than 90% complete in FAG and PU, while
over 80 and 70% of the expected species richness according to the ACE estimators were recorded
in PAS and PS, respectively (Table 1).
Habitat effect on community parameters
The four habitat categories showed significant differences in terms of species abundance, richness
and α-diversity (Table 2). Pasture obtained the highest mean values of all indexes, and LSD posthoc pair-wise tests showed that they were significantly different from the ones found in closed
habitats. Wooded habitats were not significantly different as far as richness and α-diversity were
concerned. The only difference arose when abundances were compared, with a larger number of
individuals living in beech forest than in scots or mountain pine forests. Sampling date
significantly affected α-diversity (F 11,33.59 = 3.18, P < 0.01) and species richness (F 11,33.42 = 2.75,
P < 0.05), but not abundance (F 11,33.10 = 1.04, P = 0.44). Samples conducted in the second half of
September had the smallest Shannon–Wiener and species richness mean values.
Species turnover
Species turnovers between habitats are reported in Table 3. Although Whittaker’s indexes are not
conspicuous, as expected on a small landscape scale, it is nonetheless noteworthy that the highest
values are found in the comparisons between pine forests and pasture. Instead, beech forest is
comparably different from both pasture and pine forests, as far as species composition is
concerned.
Motomura’s geometric series
Kolmogorov-Smirnov tests confirmed that the adjustment to Motomura’s geometric series model
was statistically correct in all habitats (PAS: y = 2.85−0.13x, R 2 = 0.94, d = 0.17, P > 0.20; FAG:
y = 2.64−0.20x, R 2 = 0.96, d = 0.18, P > 0.20; PS: y = 2.73−0.27x, R 2 = 0.95, d = 0.14, P > 0.20;
PU: y = 2.71−0.27x, R 2 = 0.95, d = 0.19, P > 0.20). The four regressions had homogeneous
variances (Levene test: F 3,52 = 0.26, P = 0.86). Slope comparisons are given in Fig. 2. As shown,
pasture assemblage obtained the highest evenness and pine forests the lowest; all closed habitat
assemblages are organized with fewer predominant species than pasture.
Dominance patterns
In the correspondence analysis reported in Fig. 3, axis 1, which accounted for 85.29% of inertia,
opposed the assemblages dominated by Aphodiidae to those dominated by Scarabaeidae, whereas
axis 2 distinguished assemblages with increasing Geotrupidae abundance. Samples collected in
pasture were clearly differentiated from those collected in forested habitats along axis 1, showing
that pasture assemblages had higher percentages of Scarabaeidae throughout the study period. By
comparison, closed habitats were mostly dominated by Aphodiidae and Geotrupidae and showed
an extensive degree of overlap: in these samples, Aphodiidae were consistently more numerous,
and were outnumbered by Geotrupidae only in the sample collected in scots pine forest on July
21st.
Indicator species
The hierarchical clustering conducted on the basis of Scarabaeoidea assemblage composition
(Fig. 4) identified the three forested habitats as strictly associated, with the two pine forests being
closely related. With the IndVal methodology, no indicator species for any of the three categories
of forest were found. Instead, Calamosternus granarius (Aphodiidae) was assessed as a good
indicator of forested habitats. Pasture, on the contrary, was clearly differentiated from closed
habitats, and was significantly selected by 11 species (1 Geotrupidae, 4 Scarabaeidae, 6
Aphodiidae). Finally, 5 species (3 Geotrupidae, 2 Aphodiidae) were assessed as generalists with
respect to the considered habitats (Fig. 4).
Discussion
Comparisons of community parameters showed that pasture sustained a dung beetle assemblage
which was clearly more diverse than those of closed habitats, with a higher number of both
species and individuals. This result was not biased by patterns of phenological variation because
the date of sampling was incorporated in the analysis. It is noteworthy that, although
Scarabaeoidea diversity has been related to altitudinal gradient (Romero-Alcaraz and Ávila 2000;
Jay-Robert et al. 2008a), in our case these differences were detected not only in comparisons
between pasture (1,000 m a. s. l.) and pine forests (1,400–1,500 m a. s. l.), but also when pasture
and beech forest, which are approximately at the same altitude, were compared. Possible
elevation-driven differences were only found when comparing abundances between closed
habitats: a larger number of individuals were collected in beech forest than in scots or mountain
pine forests. Since the abundance of dung beetles in a given site strongly depends on the quantity
of trophic resources available (Lumaret et al. 1992), it is likewise possible that beech forest
sustains higher numbers of dung beetles due to the presence of wild ungulates such as wild boars
(Sus scrofa), which are common in broad-leaved woodlands of the study area (Regione Autonoma
Valle d’Aosta 2008).
The analysis of species turnover provided further evidence that pasture was substantially
differentiated from closed habitats. Since Whittaker’s index takes into account the
presence/absence of each species (Magurran 2004), this outcome was influenced substantially by
the fact that 8 out of the 23 species collected during the entire sampling period (4 Scarabaeidae, 4
Aphodiidae, see Table 1) were only found in pasture. While the species turnover between pine
forests was negligible, the species turnover between beech forest and pine forests and between
pasture and beech forest was of approximately the same extent. Therefore, in this area the
turnover between open and closed habitats at the same elevation was comparable with variation in
species composition occurring along an altitudinal gradient of approximately 500 m within closed
habitats. This result further supports the idea that, in the Alps, the maintenance of pastures below
timberline is crucial to dung beetle biodiversity conservation.
A pattern of resource partitioning that arises from the mechanism of niche pre-emption (He and
Tang 2008) is frequently found in harsh ecosystems, where individuals compete for access to
scarce resources, and has been therefore successfully employed to explain the species-abundance
distributions of several dung beetle assemblages that rely on typically ephemeral resources
(Lumaret and Iborra 1996; Galante and Cartagena 1999; Errouissi et al. 2004). Motomura’s rankabundance geometric series is an indicator of the evenness of assemblages arising from such a
mechanism, by which a sequential colonization of species is assumed: the first species that
colonizes the assemblage pre-empts the first k fraction of the total resource; the second species
takes the k fraction of the remainder, and this partitioning process continues until the entire niche
space is filled. The more evenly structured the assemblage, the less steep the slope of the rankabundance distribution (He and Tang 2008). As expected, the rank-abundance distribution was
adequately explained by Motomura’s geometric series in all the habitats considered in this study.
However, pasture obtained the lowest slope, which indicates that it sustained an assemblage that
was significantly more evenly structured than the ones in forested habitats. The latter were
characterized by a few dominant species which appropriated most of the trophic resources,
although dominance was higher in pine forests than in beech forest: this may be additional
circumstantial evidence that beech forest provides a larger amount of resource for dung beetles
than pine forests.
Patterns of dominance of the three families in different habitats agreed with previous findings on
Scarabaeoidea habitat selection (Wassmer 1995; Barbero et al. 1999; Jay-Robert et al. 2008a).
While assemblages of forested habitats were substantially dominated by Aphodiidae, the
percentage of Scarabaeidae increased significantly in pasture samples. We suggest that this
pattern of habitat selection could be driven, at least partially, by the pedotrophic behavior of the
species. Contrary to Scarabaeidae and Geotrupidae, which typically lay their eggs in nests or egg
chambers within tunnels under the dung pad (paracoprid behavior: Hanski and Cambefort 1991),
most of Aphodiidae oviposit directly within dung pats (endocoprid behavior: Hanski and
Cambefort 1991). Due to these life history traits, Lobo and Martín-Piera (1999) suggested that
Aphodiidae may be more subject to environmental heterogeneity, and therefore be more habitat
specialist than Scarabaeidae and Geotrupidae. Furthermore, we suggest that endocoprids may
favor closed habitats because shading slows down the dehydration rate of food resources available
for free-living larvae, while paracoprid behavior may make the colonization of open habitats
easier. This hypotheses was also supported by the IndVal analysis. As a matter of fact, only two
(V. sticticus, A. fimetarius) out of 11 pasture indicator species were typical endocoprids
(Aphodiidae T. fossor and C. erraticus have an underground nesting behavior: Zunino and
Barbero 1990; Zunino et al. 1994; Dellacasa and Dellacasa 2006. R. foetens and S. porcus are
cleptocoprids of the brood masses of Geotrupidae: Paulian and Baraud 1982; Barbero pers. obs.).
Similarly, 4 out of the 5 species that were assessed as generalists (i.e., the ones that were found in
most of the traps set in the four habitats during the entire study period) nest in the soil underneath
the dung pad (A. rufipes: Klemperer 1980; Dellacasa and Dellacasa 2006. B. rufa: Borghesio and
Palestrini 2002). On the other hand, the only species that showed a strong selection toward closed
habitats (C. granarius, Aphodiidae) is known to have saprophyte habits (Dellacasa and Dellacasa
2006) and may therefore take advantage of the higher degree of humidity in forested areas.
A comprehensive faunistic study of the dung beetle community of Mont Avic Natural Park has
been ongoing since 1993 (Barbero et al. 1994; Palestrini et al. 2007–2008). Considering that over
80% of the Scarabaeoidea species recorded in the entire protected area were collected for the
present study in a single year, the mountain belt emerges as particularly important for the
conservation of Scarabaeoidea communities in this Alpine region. Since there is a limiting effect
of environmental conditions at extremely low and high altitudes (Jay-Robert et al. 1997), the
mountain belt, which lies at intermediate altitudes, could favor contact between faunas of low and
high altitudes. Moreover, dung beetles are influenced by complex interactions between various
environmental factors such as resource availability, soil type and moisture, elevation, exposure
and vegetation structure (Halffter and Matthews 1966; Doube 1987; Carpaneto et al. 2005; Kanda
et al. 2005; Jay-Robert et al. 2008a). Their diversity is thus expected to peak in areas with
diversified land mosaics (Verdú et al. 2007). In this study, we consistently detected small, but
significant differences in comparisons between dung beetle assemblages typical of beech and pine
forests. However, these differences are negligible when compared with the ones between pasture
and forested areas. Our analyses therefore contributed to the identification of two main dung
beetle ensembles (Fauth et al. 1996): a pasture ensemble, highly biodiverse and dominated by
Scarabaeidae, and a closed habitats ensemble, less structured and dominated by Aphodiidae and
Geotrupidae. Moreover, nearly half of the species collected showed a strong habitat selection
toward pasture, while only one species preferred forested areas (independently from forest type).
Therefore, we conclude that the loss of extensively exploited pastures within the mountain belt of
Alpine regions may bring about fundamental changes in dung insect communities.
The maintenance of mountain pastures has been shown to help other faunal groups besides dung
beetles: for example Laiolo and Rolando (2005) showed that birds typical of ecotone habitats
favor forest plots located at the border of pastures, a positive edge effect (Odum 1971) that never
occurs in transitions between forests and intensively altered open areas such as sky runs.
Furthermore, pastures within forested areas are colonized by species that are typical of open
habitats, such as many Orthoptera and Lepidoptera (Dolek and Geyer 1997; Wettstein and
Schmid 1999); in areas with a long history of land use by humans, the persistence of many
species depends upon an appropriate regulation of land use in the landscape mosaic (Verdú et al.
2007). We can therefore conclude that, in Alpine regions, low-impact grazing activities below the
timberline should be maintained, given its appropriate management and protection policies. To
achieve this goal, protected areas should adopt specific grazing plans (Gusmeroli 2004;
Gusmeroli et al. 2005). Avoiding the problems connected with intensive agricultural management
(Hutton and Giller 2003) and overgrazing (Dolek and Geyer 1997; Gusmeroli 2004; Negro et al.
2007), this approach will help maintain ecomosaic complexity and will enhance the species
turnover rate across habitats (Halffter 2002), eventually conserving biodiversity through
sustainable land use.
Acknowledgments
We are grateful to Claudia Tocco, Teresa Petrone and Elio Cannarsa, who contributed to
fieldwork and beetle identification; Matteo Negro, Enrico Caprio and Sergio Castellano for
discussions and useful suggestions on data analysis; Enrico Barbero for assistance with beetle
identification; Angela Roggero, who helped with lab facilities, and two anonymous reviewers that
helped us improve an earlier version of the manuscript. The staff of Mont Avic Natural Park (and
especially Massimo Bocca, Ermanno Broglia and Luca Ganis) gave fundamental assistance
during the fieldwork and provided the cartography used in the study. Ottavio Janni revised
English. The work was supported by the EU project Interreg IIIA ALCOTRA (COGEVAVAHSA).
References
Barbero E, Palestrini C, Zucchelli M (1994) Il popolamento di Scarabaeoidea coprofagi (Insecta:
Coleoptera) del Parco Naturale del Mont Avic (Valle d’Aosta, Italia). Rev Valdotaine Hist Nat
48:5–28
Barbero E, Palestrini C, Rolando A (1999) Dung beetle conservation: effects of habitat and
resource selection (Coleoptera: Scarabaeoidea). J Insect Conserv 3:75–84.
Biström O, Silfverberg H, Rutanen I (1991) Abundance and distribution of coprophilous Histerini
(Histeridae) and Onthophagus and Aphodius (Scarabaeidae) in Finland (Coleoptera). Entomol
Fenn 2:53–66
Borghesio L, Palestrini C (2002) Reproductive behaviour and larval development in Agrilinus
rufus (Moll, 1792) and Oromus alpinus (Scopoli, 1763) (Coleoptera: Scarabaeoidea: Aphodiidae).
Elytron 16:73–79
Borghesio L, Palestrini C, Passerin d’Entrèves P (2001) The dung beetles of the Gran Paradiso
National Park: a preliminary analysis (Insecta: Coleoptera: Scarabaeoidea). J Mt Ecol 6:41–48
Broggi MF (1995) Über die acht Thesen zu Tun und Unterlassen in den Alpen. In: CIPRA
International (ed) Tun und Unterlassen: Elemente für eine nachhaltige Entwicklung in den Alpen.
Schriftenreihe der CIPRA 13, pp 41–53
Broglio M (1996) Il Parco Regionale del Mont Avic. In: Environnement. Ambiente e territorio in
Valle d’Aosta.
Carpaneto GM, Mazziotta A, Piattella E (2005) Changes in food resources and conservation of
scarab beetles: from sheep to dog dung in a green urban area of Rome (Coleoptera,
Scarabaeoidea). Biol Conserv 123:547–556.
Chauchard S, Carcaillet C, Guibal F (2007) Patterns of land-use abandonment control treerecruitment and forest dynamics in mediterranean mountains. Ecosystems 10:936–948.
Colwell RK (2006) EstimateS: Statistical estimation of species richness and shared species from
samples.
Cremonese E, Morra di Cella U, D’Amico M (2007) Gli ambienti forestali del Parco Naturale
Mont Avic. Parco Naturale Mont Avic, Champdepraz
Dellacasa G, Dellacasa M (2006) Fauna d’Italia, vol XLI. Coleoptera Aphodiidae Aphodiinae.
Calderini, Bologna
Dolek M, Geyer A (1997) Influence of management on butterflies of rare grassland ecosystems in
Germany. J Insect Conserv 1:125–130.
Doube BM (1987) Spatial and temporal organization in communities associated with dung pats
and carcasses. In: Gee JHR, Giller PS (eds) Organization of communities: past and present.
Blackwell, Oxford, pp 255–280
Dufrêne M (2004) Program IndVal version 2.1
Dufrêne M, Legendre P (1997) Species assemblages and indicator species definition: the need of
an asymmetrical and flexible approach. Ecol Monogr 67:345–366
Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of
behavioural and evolutionary ecology studies. Anim Behav 70:967–971.
Errouissi F, Jay-Robert P, Lumaret JP, Piau P (2004) Composition and structure of dung beetle
(Coleoptera: Aphodiidae, Geotrupidae, Scarabaeidae) assemblages in mountain grasslands of the
Southern Alps. Ann Entomol Soc Am 97:701–709.
Farina A (1991) Recent changes of the mosaic patterns in a montane landscape (north Italy) and
consequences on vertebrate fauna. In: Baudry J, Bunce RGH (eds) Land abandonment and its role
in conservation. CIHEAM-IAMZ, Zaragoza, pp 121–134
Fauth JE, Bernardo J, Camara M, Resetarits WJ Jr, Van Buskirk J, McCollum SA (1996)
Simplifying the jargon of community ecology: a conceptual approach. Am Nat 147:282–286.
Fincher GT (1981) The potential value of dung beetles in pastures ecosystems. J Ga Entomol Soc
16:316–333
Galante E, Cartagena MC (1999) Comparison of mediterranean dung beetles (Coleoptera:
Scarabaeoidea) in cattle and rabbit dung. Environ Entomol 28:420–424
Giupponi C, Ramanzin M, Sturaro E, Fuser S (2006) Land use change, biodiversity and
agricultural policy in the Belluno province, Italy. Environ Sci Policy 9:163–173.
Gusmeroli F (2004) Il piano di pascolamento: strumento fondamentale per una corretta gestione
del pascolo. In: Società per lo Studio e la Valorizzazione dei Sistemi Zootecnici Alpini (ed)
Quaderni SoZooAlp 1, pp 27–41.
Gusmeroli F, Della Marianna G, Arosio G, Bozzoli L (2005) I pascoli dell’Alta Valtellina.
Presentazione di una trilogia. In: Società per lo Studio e la Valorizzazione dei Sistemi Zootecnici
Alpini (ed) Quaderni SoZooAlp 2, pp 89–96.
Halffter G (2002) Conservación de la Biodiversidad en el Siglo XXI. Bol Soc Entomol Aragonesa
31:1–7
Halffter G, Matthews EG (1966) The natural history of dung beetles of the subfamily
Scarabaeinae (Coleoptera: Scarabaeidae). Fol Entomol Mex 12–14:1–312
Hanski I, Cambefort Y (1991) Dung beetle ecology. Princeton University Press, New Jersey He
F, Tang D (2008) Estimating the niche preemption parameter of the geometric series. Acta Oecol
33:105–107.
Höchtl F, Lehringer S, Konold W (2005) “Wilderness”: what it means when it becomes a
reality—a case study from the southwestern Alps. Landsc Urban Plan 70:85–95.
Hutton SA, Giller PS (2003) The effects of the intensification of agriculture on northern
temperate dung beetle communities. J Appl Ecol 40:994–1007.
Jay-Robert P, Lobo JM, Lumaret JP (1997) Altitudinal turnover and species richness variation in
European montane dung beetle assemblages. Arct Alp Res 29:196–205.
Jay-Robert P, Lumaret JP, Lebreton JD (2008a) Spatial and temporal variation of mountain dung
beetle assemblages and their relationships with environmental factors (Aphodiinae: Geotrupinae:
Scarabaeinae). Ann Entomol Soc Am 101:58–69.
Jay-Robert P, Niogret J, Errouissi F, Labarussias M, Paoletti É, Vázquez-Luis M, Lumaret JP
(2008b) Relative efficiency of extensive grazing vs. wild ungulates management for dung beetle
conservation in a heterogeneous landscape from Southern Europe (Scarabaeinae, Aphodiinae,
Geotrupinae). Biol Conserv 141:2879–2887.
Kanda N, Yokota T, Shibata E, Sato H (2005) Diversity of dung-beetle community in declining
Japanese subalpine forest caused by an increasing sika deer population. Ecol Res 20:135–141.
Klemperer HG (1980) Kleptoparasitic behaviour of Aphodius rufipes (L.) larvae in nests of
Geotrupes spiniger Marsh. (Coleoptera, Scarabaeidae). Ecol Entomol 7:69–83.
Laiolo P, Rolando A (2005) Forest bird diversity and ski-runs: a case of negative edge effect.
Anim Conserv 7:9–16.
Laiolo P, Dondero F, Ciliento E, Rolando A (2004) Consequences of pastoral abandonment for
the structure and diversity of the alpine avifauna. J Appl Ecol 41:294–304.
Levene H (1960) Robust tests for equality of variances. In: Olkin I, Ghurye SG, Hoeffding W,
Madow WG, Mann HB (eds) Contributions to probability and statistics: essays in honor of Harold
Hotelling. Stanford University Press, Menlo Park, pp 278–292
Lichtenberger E (1994) Die Alpen in Europa. Veröffentlichungen der Kommission für
Humanökologie 5. Gefährdung und Schutz der Alpen. Österreichische Akademie der
Wissenschaften, Wien, pp 53–86
Lobo JM, Martín-Piera F (1999) Between-group differences in the Iberian dung beetle species–
area relationship (Coleoptera: Scarabaeidae). Acta Oecol 20:587–597.
Lobo JM, Martín-Piera F, Veiga CM (1988) Las trampas pitfall con cebo, sus posibilidades en el
estudio de las comunidades coprófagas de Scarabaeoidea (Col.). I. Características determinantes
de su capacidad de captura. Rev Ecol Biol Sol 25:77–100
Lumaret JP (1990) Atlas des Coleoptères Scarabeides Laparosticti de France. Série Inventaires de
Faune et de Flore, fascicule 1. Secrétariat de la Faune et de la Flore, Paris
Lumaret JP, Iborra O (1996) Separation of trophic niches by dung beetles (Coleoptera,
Scarabaeoidea) in overlapping habitats. Pedobiologia (Jena) 40:392–404
Lumaret JP, Kirk A (1991) South temperate dung beetles. In: Hanski I, Cambefort Y (eds) Dung
beetle ecology. Princeton University Press, Oxford, pp 97–115
Lumaret JP, Kadiri N, Bertrand M (1992) Changes in resources: consequences for the dynamics
of dung beetle communities. J Appl Ecol 29:349–356.
Magurran AE (2004) Measuring biological diversity. Blackwell, Malden
Martín-Piera F, Lobo JM (1995) Diversity and ecological role of dung beetles in Iberian grassland
biomes. In: MacCracken DI, Bignal EM, Wenlock SE (eds) Farming on the edge: the nature of
traditional farmland in Europe. Proceedings of the fourth European forum on nature conservation
and pastoralism, Trujilo, Nov 1994, pp 147–153
Martín-Piera F, López-Colón JI (2000) Coleoptera, Scarabaeoidea I. Fauna Ibérica, vol 14. Museo
Nacional de Ciencias Naturales, Madrid
McGeoch MA, Van Rensburg BJ, Botes A (2002) The verification and application of
bioindicators: a case study of dung beetles in a savanna ecosystem. J Appl Ecol 39:661–672.
Milestad R, Hadatsch S (2003) Organic farming and social-ecological resilience: the alpine
valleys of Sölktäler, Austria. Conserv Ecol 8(1):3.
Motomura A (1932) Statistic analysis of community. Anim Mag 44:379–383
Negro M, Casale A, Migliore L, Palestrini C, Rolando A (2007) The effect of local anthropogenic
habitat heterogeneity on assemblages of carabids (Coleoptera, Caraboidea) endemic to the Alps.
Biodivers Conserv 16:3919–3932.
Nichols E, Spector S, Louzada J, Larsen T, Amequita S, Favila ME (2008) Ecological functions
and ecosystem services provided by Scarabaeinae dung beetles. Biol Conserv 141:1461–1474.
Numa C, Verdú JR, Sánchez A., Galante E (2009) Effect of landscape structure on the spatial
distribution of Mediterranean dung beetle diversity. Div Distrib 15:489–501.
Odum EP (1971) Fundamentals of ecology. Saunders, Philadelphia
Palestrini C, Roggero A, Negro M, Quaglia E, Rovei R, Barbero E (2007–2008) Studio sulla
coleotterofauna coprofaga (Coleoptera: Scarabaeoidea) nel Parco Naturale Regionale Mont Avic
(Valle d’Aosta, Italia). Rev Valdotaine Hist Nat 61–62:189–217
Paulian R, Baraud J (1982) Faune des Coléoptères de France, II: Lucanoidea et Scarabaeoidea.
Encyclopédie Entomologique, vol 43. Lechevalier, Paris
Regione Autonoma Valle d’Aosta (2008) Piano regionale faunistico venatorio per il periodo
2008–2012. Assessorato Agricoltura e Risorse Naturali, Dipartimento Risorse Naturali e Corpo
Forestale, Direzione Flora, Fauna, Caccia e Pesca, Aosta
Romero-Alcaraz E, Ávila JM (2000) Effect of elevation and type of habitat on the abundance and
diversity of Scarabaeoid dung beetle (Scarabaeoidea) assemblages in a Mediterranean area from
Southern Iberian Peninsula. Zool Stud 39:351–359
Roslin T, Koivunen A (2001) Distribution and abundance of dung beetles in fragmented
landscapes. Oecologia 127:69–77.
Verdú JR, Moreno CE, Sanchez-Rojas G, Numa C, Galante E, Halffter G (2007) Grazing
promotes dung beetle diversity in the xeric landscape of a Mexican Biosphere Reserve. Biol
Conserv 140:308–317.
Wassmer T (1995) Selection of the spatial habitat of Coprophagous beetles in the Kaiserstuhl area
near Freiburg (SW-Germany). Acta Oecol 16:461–478
Wettstein W, Schmid B (1999) Conservation of arthropod diversity in montane wetlands: effect
of altitude, habitat quality and habitat fragmentation on butterflies and grasshoppers. J Appl Ecol
36:363–373.
Whittaker RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr
30:279–338.
Zunino F (1980) Wilderness. Una nuova esigenza di conservazione delle aree naturali. Collana
Verde, vol 51. Ministero dell’agricoltura e delle foreste, Roma
Zunino M, Barbero E (1990) Food relocation and the reproductive biology of Aphodius fossor
(L.) (Coleoptera, Scarabaeidae, Aphodiinae). In: Abstracts of the thirteenth meeting of the Italian
Society for the Study of Animal Behaviour, Perugia, Italy, 25–27 May 1989. Ethol Ecol Evol
2:334
Zunino M, Canino L, Coletta E (1994) Feeding and nesting behaviour of Aphodius
(Colobopterus) erraticus (L.). In: Abstracts of the fifteenth meeting of the Italian Society for the
Study of Animal Behaviour, Castiglione della Pescaia, Italy, 22–24 Sept 1992. Ethol Ecol Evol
6:451–452
Fig. 1
Sampled localities within Mont Avic Natural Park and the adjacent areas of Val Chalamy.
Transect locations are indicated with PU, PS, PAS and FAG depending on the habitat sampled.
Distribution of cover types are shown
Table 1
Specimens sampled and total number of species expected for each habitat according to the
abundance-based richness estimator (ACE)
No. individuals trapped
Species
PS
PU FAG PAS
Geotrupidae
Anoplotrupes stercorosus (Scriba, 1796)
143
55
132
68
Geotrupes spiniger (Marsham, 1802)
11
13
13
51
Geotrupes stercorarius (Linnaeus, 1758)
7
8
3
124
Euoniticellus fulvus (Goeze, 1777)
–
–
–
59
Onthophagus coenobita (Herbst, 1783)
–
–
2
1
Onthophagus fracticornis (Preyssler, 1790) 15
8
29
1,081
Onthophagus joannae (Goljan, 1953)
–
–
–
114
Onthophagus taurus (Schreber,1759)
–
–
–
32
Onthophagus vacca (Linnaeus, 1767)
–
–
–
2
Acrossus depressus (Kugelann, 1792)
–
–
23
4
Acrossus rufipes (Linnaeus, 1758)
275
256
563
445
Aphodius fimetarius (Linnaeus, 1758)
–
–
–
61
Bodilopsis rufa (Moll, 1782)
49
191
61
142
Calamosternus granarius (Linnaeus, 1767) 41
27
24
2
Colobopterus erraticus (Linnaeus, 1758)
–
–
–
30
Limarus zenkeri (Germar, 1813)
52
45
92
30
Otophorus haemorrhidalis (Linnaeus, 1758) –
–
–
1
Parammoecius corvinus (Erichson, 1848)
1
1
–
1
Planolinus fasciatus (Oliver, 1789)
1
–
1
1
Rhodaphodius foetens (Fabricius, 1787)
–
–
–
14
Sigorus porcus (Fabricius, 1792)
–
–
1
13
Teuchestes fossor (Linnaeus, 1758)
–
–
3
50
Volinus sticticus (Panzer, 1798)
–
–
16
50
Total abundance
595
604
963
2,376
Observed species richness
10
9
14
23
ACE
14.07 9.52 15.25 28.14
Inventory completeness (%)
71.07 94.54 91.80 81.73
Scarabaeidae
Aphodiidae
Inventory completeness is observed richness as a percentage of total expected richness (ACE)
Table 2
Mean ± SE of alpha diversity (Shannon Wiener), species richness and abundance of
Scarabaeoidea assemblages per habitat
PS
PU
FAG
PAS
Habitat effect
Alpha diversity 0.71 ± 0.06a 0.76 ± 0.06a 0.77 ± 0.06a 1.32 ± 0.04b F 3,33.86 = 18.03*
Abundance
8.88 ± 0.85d 8.51 ± 0.93d 15.53 ± 2.03e 34.94 ± 3.39f F 3,33.15 = 9.01*
Species richness 2.67 ± 0.20g 2.66 ± 0.18g 3.16 ± 0.26g 6.25 ± 0.25h F 3,33.62 = 28.94*
Inter-habitat differences were tested with a two-way ANOVA holding sample date as a random
factor
Least-squares deviation (LSD) post-hoc tests were used for pair-wise comparisons of means.
Within each line values followed by the same letter are not significantly different from each other
(P > 0.05)
* P < 0.01
Table 3
Beta diversity (β w)
PS
PU
PU FAG
0.05
FAG 0.25 0.30
PAS 0.39 0.44 0.24
Species turnovers (Whittaker’s index) between habitats are reported
Fig 2. Rank-abundance plot. The lower the slope of each regression line, the greater the evenness
of the assemblage. Results of pair-wise comparisons between habitats are given in the table
Fig. 3 Correspondence analysis of dung beetle assemblages as a function of relative percentages
of families sampled. Beetles trapped in the same habitat on each sample day were pooled for the
analysis. Axis 1 opposes the assemblages dominated by Aphodiidae (mostly sampled in forested
habitats) to those dominated by Scarabaeidae (exclusively collected in pasture). Axis 2
distinguishes assemblages with increasing abundance of Geotrupidae
Fig. 4
Indicator species associated with different nodes of the habitat cluster. Euclidean linkage
distances are reported. The indicator value (0–100) is given in parentheses. All species presented
are significant indicators (P < 0.05)

Download Report