JOURNAL OF ECOTOURISM

https://doi.org/10.1080/14724049.2020.1772798

A first step to evaluate the impact of ecotourism on

biodiversity in El Salvador: a case study using dung beetles in
a National Park
a a b
José D. Pablo-Cea , Maryory A. Velado-Cano and Jorge Ari Noriega
aEscuela de Biología, Facultad de Ciencias Naturales y Matemática, Universidad de El Salvador, San Salvador,
El Salvador; bDepartamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias Naturales (CSIC),
Madrid, España

ABSTRACT ARTICLE HISTORY

Ecotourism involves visiting natural areas without adversely Received 8 March 2019
affecting biodiversity, an objective that is often not reached. Accepted 19 May 2020
Although ecotourism in El Salvador is currently under-developed,
KEYWORDS
it has been proposed for the conservation of forests that remain Conservation; protected
within the territory. To this respect, National Park El Imposible is areas; indicator species;
the largest natural protected area in the nation, with 23% of its Scarabaeidae; National Park
extension designated for ecotourism. The objective of this study El Imposible
was to evaluate the impact of ecological disturbances produced
by ecotourism, using dung beetles as biological indicators in the
park. Three zones differing in tourism intensity: conservation,
extensive, and intensive, were evaluated. Six samplings using
pitfall traps were carried out from June–November, 2013 in each
zone. We recorded a significantly lower beetle abundance in the
intensive-use zone, even though biomass tended to increase with
ecotourism intensity due to proportional increase in large-sized
species. There were differences in composition, diversity, and
evenness of the dung beetle assemblage, evidencing ecological
disturbances in the intensive-use zone. Ecotourism in the park has
caused a negative impact on the dung beetle assemblage
structure due to the loss of habitat specialists in favor of
widespread generalists. Consequently, ecotourism should be
regulated to minimize its effects in the site.

Introduction
Ecotourism pursues the economic exploitation of wildlife and natural environments,
focusing mainly on protected areas with conserved habitats (Lira & Naranjo, 2003).
The precise definition of this activity is ambiguous, but terms like: ‘nature based’, ‘preser-
vation’, ‘ethics’, and ‘education’ are commonly associated (Donohoe & Needham, 2008).
According to an idealized notion, it is: ‘an environmentally responsible journey, where
relatively undisturbed areas are visited for the purpose of enjoying and appreciating
nature, promoting conservation’ (Ceballos-Lascuráin, 1996). It is considered to be an
activity with a low impact on nature, representing a balance between conservation

CONTACT José D. Pablo-Cea jose.pablo@ues.edu.sv Escuela de Biología, Facultad de Ciencias Naturales y Mate-
mática, Universidad de El Salvador, Final 25 Avenida Norte, San Salvador, El Salvador
© 2020 Informa UK Limited, trading as Taylor & Francis Group
2 J. D. PABLO-CEA ET AL.

strategies and socio-economic benefits for local populations (Ceballos-Lascuráin, 1996),

which leads to the challenge of finding mechanisms that promote coexistence between
humans and wildlife (Heil et al., 2007; Wolf et al., 2019). Despite this, ecotourism can
negatively affect the ecosystem in different ways. For instance, actions like hunting,
human trampling, and trash dumping cause unintended disturbances like habitat altera-
tion and pollution (Buckley, 2011; Buckley et al., 2016; Geffroy et al., 2015; Krüger, 2005).
Factors such as the type of activity performed, the behavior of tourists, the frequency and
magnitude of visitation, determine the response of wildlife to ecotourism and delimitate its
consequent sustainability (Buckley, 2011; Krüger, 2005).
The extent of ecotourism in Central American countries is variable. It ranges from
countries such as Costa Rica that focus a large part of their economy on this activity
(Krüger, 2005; Weaver, 1999), to countries like El Salvador where ecotourism programs
are still not well established and studies evaluating the impact of this activity on biodiver-
sity have yet to be carried out. Despite this fact, for a developing country like El Salvador,
ecotourism represents a useful conservation strategy to protect the few forest fragments
that still remain (Buckley, 2011; Dull, 2008). For instance, in El Salvador less than 2%
of its original forest cover remains. The country’s land use is a mosaic of agricultural,
abandoned coffee plantations and urban landscapes (Crespin & Simonetti, 2016; Dull,
2008; Monro et al., 2006). Immersed in this context, the National Park El Imposible
(NPEI) is the largest and most diverse protected area in the nation (SalvaNatura, 2016;
USAID, 2010). The extension of the park is 4000 ha, with 23% of its area designated for
tourism. This activity supports local tour guides and merchants of the informal sector
that depend on selling goods to tourists to subsist (SalvaNatura, 2016). Among the
different types of ecosystems that can be used for ecotourism, natural areas and National
Parks should have the most restrictions that favor low-impact activities, in order to protect
biodiversity (Buckley, 2011). Consequently, an evaluation of the effect of ecotourism on
the biodiversity of such an important area to El Salvador is a priority. In this regard,
the use of ecological indicators allows for the quantification of human impacts and
their consequences on ecosystems, revealing the efficacy of the sustainability strategies
implemented up to that moment (Baral, 2015; Lucrezi et al., 2009).
Dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) are an effective indicator of the
intensity of various factors that affect biodiversity, including: landscape fragmentation,
logging, hunting of mammals and changes in land use (Bicknell et al., 2014; Nichols
et al., 2007; Nichols et al., 2009; Noriega et al., 2012; Quintero & Halffter, 2009). Addition-
ally, they are a group with a stable taxonomy, are widely distributed, and have a close
relationship with the health of mammal populations since any change in the quality or
quantity of available excrement affects the structure of the beetle species assemblage
(Halffter & Favila, 1993; Nichols et al., 2007, 2009; Spector, 2006). These beetles are
classified into three main functional groups depending on the type of relocation of their
food resource (i.e. paracoprids, beetles that dig tunnels below the excrement pile and relo-
cate portions of the dung vertically; telecoprids, beetles that make excrement balls and roll
them horizontally; and endocoprids, beetles that live inside the dung pile their entire life
cycle), and some species can even feed on other resources than dung such as carrion, fungi,
fruit, and decaying plant material (Arnett et al., 2002).
The objective of this work was to study the ecological disturbances produced by eco-
tourism in NPEI in El Salvador. We predicted that in zones with greater tourism, there
 JOURNAL OF ECOTOURISM 3

would be a negative effect on dung beetle diversity and assemblage structure. To test our
hypothesis, we analyzed changes in dung beetle assemblages (i.e. richness, abundance,
diversity, composition, evenness, biomass, and food relocation guild structure), and inter-
preted these factors as indicators of the degree of ecological disturbance produced by eco-
tourism in three intensity zones. With this work we intend to take the first step toward the
development of sustainable ecotourism activity in this protected area.

Material and methods

Study area
The NPEI (13°48′00.97” -13°48′00.97” N a 89°53′41.93”- 89°53′41.93” W) is located in the
Department of Ahuachapán, in the southwest of El Salvador (Figure 1). The park has a
total area of 4000 ha, being the largest conserved area in the country (USAID, 2010).
The dominant vegetation type is Tropical Dry Forest with a marked seasonal regime of
six months of rain (May to October) and six months of dry season (November to April),
with an annual average rain- fall of 2000 mm. The woody dominant plant species
recorded during sampling at the study sites were: Copalchi (Alstonia longifolia), Marillo
(Calophyllum brasiliense), Storax (Clethra mexicana), Spanish elm (Cordia alliodora),
Copalchi (Croton reflexifolius), Alu- minio (Drypetes lateriflora), West Indian Elm
(Guazuma ulmifolia), Mulo (Licania retifo- lia), Escobo (Maytenus chiapensis), Sweet
Pea (Phoebe sp.) and Capulin (Trema micrantha). Among the most abundant mammals
in the park are: Central American Agouti (Dasyprocta punctata), Lowland Paca
(Cuniculus paca), Nine-banded Armadillo

Figure 1. (A) Location of the three sampling zones (low tourism – LTZ, medium tourism – MTZ, and
high tourism – HTZ) at NP El Imposible, Department of Ahuachapán, El Salvador, and (B) sampling dis-
position of the linear transects, pitfall traps, and baits in each zone.
4 J. D. PABLO-CEA ET AL.

(Dasypus novemcinctus), White-nosed Coati (Nasua narica), and White-tailed Deer (Odo-
coileus virginianus) (Rodríguez, 2003; Velado-Cano, 2014).

Zones and sampling sites

The park receives approximately 6500 visitors per year and is divided into three zones
according to their number of visitors: conservation, extensive, and intensive (SalvaNatura,
2016). In order to understand the effect of ecotourism in the Park, one site was selected for
monitoring within each zone, according to the number of visitors, accessibility, and plant
structure. Due to limitations in the number of rangers in the park that could supervise the
research activities and give security, repetitions were not possible. The three selected sites
are located in an altitudinal range between 760 and 960 m in elevation, with an average
DBH (i.e. diameter at breast height) between 0.75 and 0.82 cm, and a canopy coverage
between 52% and 60%.

(A) Conservation use zone (low tourism – LTZ): covers 77% of the park’s extension. This
zone is not intended for tourism and is used for conservation. Only park rangers can
access the area, although researchers are also admitted with prior authorization. The
chosen location was La Timbona: 13°49′52.5′′ N–89°56′09.8′′ W. Park rangers per-
formed an average of 100 monitoring walks per year in this zone (0.27 persons per
day).
(B) Extensive use zone (medium tourism – MTZ): covers 17% of the park’s extension.
This zone is destined to ecological educational walks, admitting an average of 500
tourists per year (1.36 persons per day). The chosen location was Cerro Dávila: 13°
49′59.2′′ N–89°57′02.1′′ W. This zone is a route that few visitors use.
(C) Intensive use zone (high tourism – HTZ): covers 6% of the park’s extension. In this
zone tourist recreation and environmental education are encouraged, admitting an
average of 6000 tourists per year (16.4 persons per day). The chosen location was
Cerro El Mulo: 13°49′36.1′′ N–89°56′44.0′′ W. This zone is the route used by most
tourists entering the park.

Sampling of dung beetles

In order to understand the effect of ecotourism in the diversity and structure of the
dung beetle assemblage, six samplings were collected from June to November of 2013
under the scientific collection permission: ADEN-DA-MARN-DEV-GVS-AIMA-77-
2013. Two parallel linear transects of 500 m each (Noriega & Fagua, 2009) were estab-
lished in each selected site of the three zones (LTZ, MTZ, and HTZ; Figure 1) along the
main, most heavily trafficked path. The transects were separated 50 m from the main
trail and 100 m from each other, in order to avoid interference in the trap efficiency
(see Larsen & Forsyth, 2005). In each transect, 10 pitfall traps were placed intercalated:
five baited with 60 g of fresh human dung and five traps baited with 60 g of decaying
chicken carcass (Noriega & Fagua, 2009). The pitfall traps consisted in a plastic bottle of
2.5 L (34 × 8 × 5 cm) that was split into halves. In the upper half a second cut was made
to increase its aperture, in order to allow larger sized beetles to easily enter. Then the
 JOURNAL OF ECOTOURISM 5

upper half of the cut bottle was inverted and placed inside the lower half like a funnel.
A bent wire in an inverted ‘U’ shape was placed above the trap supporting the bait (see
Pablo-Cea 2013). Above the bait, a white dish (Ø 22 cm) was placed to prevent drying
or flooding by rain. The traps remained active for a period of 72 h. The collected speci-
mens were stored in vials with 70% alcohol and transported to the Entomology Labora-
tory of the School of Biology at the University of El Salvador. The beetles were
identified at the species level using different taxonomic keys (Edmonds, 1994;
Edmonds & Zidek, 2010; Génier, 2009; Halffter & Martínez, 1977; Howden & Young,
1981; Kohlmann, 1984; Kohlmann & Solís, 1997, 2001; Solís & Kohlmann, 2002,
2013; Vaz de Mello et al., 2011) under the advisory of Ángel Solís from the National
Museum of Costa Rica.

Data analysis
Species accumulation curves were generated using the Chao 1, ACE, and Jacknife 2 indi-
cators in EstimateS v 9.1 (Colwell, 2016). Diversity was calculated using the Shannon–
Wiener index (H). The biomass of each species was estimated following the methodology
proposed by Lobo (1993). To calculate the similarity between the species composition
registered in each site, analyses of similarity (Jaccard and Simpson indexes) were per-
formed in Past v 3.0.1. A Shapiro–Wilks test was performed to test normality. To deter-
mine if there were significant differences between localities and quantified variables, an
analysis of variance (ANOVA) was performed. To detect significant differences in the
ANOVA, the Tukey HSD post-hoc test was used. All statistical tests were performed in
Statistica v. 6.0. In order to find indicator species for each of the sites, the IndVal index
was calculated (Dufrêne & Legendre, 1997) in R (R Core Team, 2013). All analyses,
except richness indicators, were carried out using 21 species. This is because, in the
field, all the individuals of the Uroxys genus were grouped together assuming that they
belonged to a single species. We made this assumption due to the restrictions in the col-
lection permit, which did not allow for the collection of all of the captured specimens.
Therefore, the individuals of Uroxys were separated into two different species after
identification (see Table 1). Additionally, we classified beetle species as coprophagous
or necrophagous according to the proportion of individuals that arrived to each bait
(90% of the specimens captured in one or the other bait), and into traditional relocation
guilds (i.e. tunnelers, rollers, and dwellers) following the available information for each
genus and species (Edmonds, 1994; Edmonds & Zidek, 2010; Génier, 2009; Halffter &
Martínez, 1977; Howden & Young, 1981; Kohlmann, 1984; Kohlmann & Solís, 1997,
2001; Solís & Kohlmann, 2002, 2013; Vaz de Mello et al., 2011).

Results
The number and spatial distribution of the sampling units allowed for high sampling
efficiency. Most species in the zones open to tourism were captured: medium tourism –
MTZ (80.16–91.90%) and high tourism – HTZ (78.35–84.25%). However, in the conser-
vation zone, the indicators used (ACE, Chao 1, and Jack 2) estimated that less than 70% of
the existing species were collected (low tourism – LTZ, 55.9–69.19%).
6 J. D. PABLO-CEA ET AL.

Table 1. Dung beetles collected in the three samplings zones (low tourism – LTZ, medium tourism –
MTZ, and high tourism – HTZ), at NP El Imposible, Department of Ahuachapán, El Salvador. Fg
(Functional group): Paracoprids (P), Telecoprids (T), and Endocoprids (E). Bp (Bait preferences):
Coprophagy (C), Necrophagy (N), and Generalist (G).
Species Fg Bp Sites (tourism level) Total
Tribe LTZ MTZ HTZ
Ateuchini Ateuchus rodriguezi (Preudhomme de Borre, 1886) P – 1 0 0 1
Uroxys spp.a P C 858 135 43 1036
Coprini Canthidium pseudopunticolle Solís and Kohlmann, 2004 P C 234 114 31 379
Copris costaricensis Gahan, 1894 P C 36 18 19 73
Copris lugubris Boheman, 1858 P C 9 3 12 24
Dichotomius annae Kohlmann & Solís, 1997 P – 0 1 1 2
Dichotomius centralis (Harold, 1869) P C 19 14 69 102
Dichotomius yucatanus (Bates, 1887) P C 21 8 56 85
Deltochilini Canthon cyanellus LeConte, 1859 T – 1 0 1 2
Canthon femoralis Chevrolat, 1834 T C 263 1096 28 1387
Canthon sp. 1 T – 1 5 1 7
Deltochilum gibbosum Bates, 1887 T – 1 1 4 6
Oniticellini Eurysternus magnus Laporte, 1840 E C 0 7 0 7
Onthophagini Onthophagus batesi Howden and Cartwright, 1963 P C 6 3 18 27
Onthophagus belorhinus (Bates, 1887) P G 410 602 296 1308
Onthophagus landolti Harold, 1880 P C 1895 979 488 3362
Phanaeini Coprophanaeus corythus (Harold, 1863) P N 29 46 63 138
Phanaeus endymion Harold, 1863 P G 7 11 6 24
Phanaeus eximius Bates, 1887 P – 1 0 0 1
Phanaeus wagneri Harold, 1863 P – 7 0 0 7
Sisyphini Sisyphus mexicanus Harold, 1863 T – 1 0 0 1
Abundance 3800 3043 1136 7979
Richness 19 16 16 22
Shannon index (H ) 1.47 1.51 1.75 –
Evenness (%) 50 54 63 –
a
This species-complex correspond to: Uroxys deavilai Delgado and Kohlmann, 2007 and U. microcularis Howden and Young,
1981.

Assemblage structure, guilds, biomass, and localities

A total of 22 species of dung beetles were collected, distributed in 11 genera (Table 1). The
species with the highest relative abundance were: Onthophagus landolti (n = 3362,
42.14%), Canthon femoralis (n = 1387, 17.38%), and Onthophagus belorhinus (n = 1308,
16.39%). A total of 7979 individuals were collected throughout the whole period, with Sep-
tember and August being the months with highest abundance (Figure 2(A)) and July the
month with the greatest richness (Figure 2(B)). The tunnelers registered 16 species (n =
6569, 82.32%), rollers five species (n = 1403, 17.58%), and dwellers only one species (Eur-
ysternus magnus; n = 7, 0.08%) (Table 1). In general, a total of 111.51 g (dry weight) of
biomass was obtained, in which Coprophanaeus corythus was the species that recorded
the highest contribution with 56.58 g (50.74%), followed by Dichotomius centralis with
16.11 g (14.45%), and O. belorhinus with 9.01 g (8.08%) (Table 2).
In the LTZ, 19 species and 3800 individuals were collected (n = 3564 – 93.79% in dung
and n = 236 – 6.21% in carrion) (Table 1). The species with the highest abundance were
O. landolti (n = 1895, 49.87%) and Uroxys spp. (n = 858, 22.58%). A total of 29.10 g
(26.09%) was obtained, of which 11.89 g (40.84%) belonged to C. corythus and 4.28 g
(14.70%) to O. landolti (Table 2). In the MTZ, 16 species and 3043 individuals were col-
lected (n = 2558 – 84.06% in dung and n = 485 – 15.94% in carrion) (Table 1). The species
with the highest abundance were: C. femoralis (n = 1096, 36.02%) and O. landolti (n = 979,
 JOURNAL OF ECOTOURISM 7

Figure 2. Diversity of dung beetles by: (A) abundance, and (B) richness in pitfall traps baited with dung
and carrion during six months of sampling at NP El Imposible, Department of Ahuachapán, El Salvador.

32.17%). A total of 35.84 g (32.14%) was obtained, of which 18.86 g (52.62%) belonged to
C. corythus and 4.53 g (12.64%) to C. femoralis (Table 2). In the HTZ, 16 species and 1136
individuals were collected (n = 998 – 87.85% in dung and n = 138 – 12.15% in carrion)
(Table 1). The species with the highest abundance were: O. landolti (n = 488, 42.96%)
and O. belorhinus (n = 296, 26.06%). A total of 45.56 g of biomass was obtained, of
which 25.80 g (55.48%) belonged to C. corythus and 10.90 g (23.41%) to D. centralis
(Table 2).

Bait preferences
Eight species (36.36%) were recorded exclusively in dung, one (4.54%) exclusively in
carrion, and 13 (59.09%) were found in both baits (Table 1). In dung, 7120 individuals
were collected (89.23%), while in carrion 859 (10.77%). The species with the highest rela-
tive abundance in dung were O. landolti (n = 3284, 46.12%) and C. femoralis (n = 1282,
18.01%). The total biomass collected in dung was 50.71 g, of which D. centralis was the
species with the highest biomass (15 g, 29.59%), followed by O. landolti with 7.41 g
(14.62%), O. belorhinus with 6.23 g (12.29%), and C. femoralis with 5.30 g (10.45%). In
carrion, the species with the highest abundance were O. belorhinus (n = 404, 45.01%),
C. corythus (n = 133, 16.27%), and C. femoralis (n = 105, 11.39%). The total biomass
8 J. D. PABLO-CEA ET AL.

Table 2. Biomass (g) of the collected species calculated according to Lobo (1993) for one individual, for
each sampling zones (low tourism – LTZ, medium tourism – MTZ, and high tourism – HTZ), and total at
NP El Imposible, Department of Ahuachapán, El Salvador.
Biomass (g)
1 ind. Sites (tourism level) Total
Species LTZ MTZ HTZ
A. rodriguezi 0.0069 0.01 0.00 0.00 0.01
C. pseudopunticolle 0.0011 0.25 0.12 0.03 0.41
C. costaricensis 0.0308 1.11 0.56 0.59 2.25
C. lugubris 0.1307 1.18 0.39 1.57 3.14
D. annae 0.4100 0.00 0.41 0.41 0.82
D. centralis 0.1579 3.00 2.21 10.90 16.11
D. yucatanus 0.0412 0.86 0.33 2.31 3.50
C. cyanellus 0.0069 0.01 0.00 0.01 0.01
C. femoralis 0.0041 1.09 4.53 0.12 5.73
Canthon sp. 1 0.0069 0.01 0.03 0.01 0.05
D. gibbosum 0.2240 0.22 0.22 0.90 1.34
C. corythus 0.4100 11.89 18.86 25.83 56.58
P. endymion 0.1069 0.75 1.18 0.64 2.56
P. eximius 0.0686 0.07 0.00 0.00 0.07
P. wagneri 0.0863 0.60 0.00 0.00 0.60
E. magnus 0.0686 0.00 0.48 0.00 0.48
O. batesi 0.0041 0.02 0.01 0.07 0.11
O. belorhinus 0.0069 2.83 4.15 2.04 9.01
O. landolti 0.0023 4.28 2.21 1.10 7.59
S. mexicanus 0.0069 0.01 0.00 0.00 0.01
Total 29.10 35.84 46.56 111.51

collected in carrion was 60.79 g, of which C. corythus was the species with the highest
biomass represented by 54.52 g (89.69%), followed by O. belorhinus with 2.78 g
(4.58%), and D. centralis with 1.11 g (1.81%).

Tourism gradient effect and indicator values

The difference in tourist presence was found to negatively affect the abundance, and posi-
tively affect the biomass of the dung beetle assemblage, but did not show to affect its rich-
ness. The increase in the number of tourists was associated with a significant decrease in
dung beetle abundance (F = 12.59, df = 15, p < 0.001) (Figure 3(A)). The Tukey test regis-
tered differences between the HTZ and the other two zones (HTZ–-MTZ p < 0.001, HTZ–
LTZ p < 0.001), but did not detect differences between MTZ and LTZ (p = 0.643). There
were no significant differences in dung beetle richness comparing the three sites (F =
0.396, df = 15, p = 0.680) (Figure 3(B)). Significant differences were recorded in biomass
(F = 7.447, df = 15, p < 0.001) (Figure 3(C)), with the Tukey test revealing differences
between the HTZ and the other two zones (HTZ–MTZ p = 0.016, HTZ–LTZ p < 0.001),
but not between the MTZ and the LTZ (p = 0.535). This was because the dung beetle
biomass was greater in the HTZ. The species composition varied among the three
zones (Jaccard Index, Figure 4(A)); dominance remained at very similar values across
the three sites (Simpson Index, Figure 4(B)), while diversity appeared to decrease with
increasing tourism (Shannon index; LTZ = 1.75, MTZ = 1.51, HTZ = 1.47). In terms of
the main functional groups, there is no gain or loss across the three sites, but some func-
tionally important species (e.g. Phanaeus eximus, P. wagneri, and Sisyphus mexicanus) dis-
appeared with an increase in tourism (Table 1). The IndVal test identified a single species
 JOURNAL OF ECOTOURISM 9

Figure 3. Diversity comparison of the assemblage of dung beetles by: (A) abundance, (B) richness, and
(C) biomass in the three sampling zones (low tourism – LTZ, medium tourism – MTZ, and high tourism
– HTZ), at NP El Imposible, Department of Ahuachapán, El Salvador. Diferrent letters above bars indicate
significant differences α = 0.05.

as a potential indicator of the HTZ (Dichotomius yucatanus), two species as indicators of

the MTZ (C. femoralis and O. belorhinus), and two species as indicators of LTZ (Canthi-
dium pseudopunticolle and P. eximius) (Table 3).

Table 3. Indval values of the indicator species of dung beetles with high and significative scores, in the
three zones (low tourism – LTZ, medium tourism – MTZ, and high tourism – HTZ) at NP El Imposible,
Department of Ahuachapán, El Salvador.
Zone Species IndVal p-Value
LTZ C. pseudopunticolle 0.617 0.035
LTZ P. eximius 0.564 0.013
MTZ C. femoralis 0.790 0.009
MTZ O. belorhinus 0.667 0.022
HTZ D. yucatanus 0.676 0.031
10 J. D. PABLO-CEA ET AL.

Figure 4. Structure analysis of the dung beetles assemblages by: (A) Jaccard similarity index, and (B)
Simpson dominance index in the three sampling zones (low tourism – LTZ, medium tourism – MTZ, and
high tourism – HTZ), at NP El Imposible, Department of Ahuachapán, El Salvador.

Discussion
Dry forests are one of the most threatened ecosystems in the Neotropics due to multiple
anthropogenic pressures (Miles et al., 2006). In El Salvador, these pressures have been
exacerbated and forests are now very scarce (Dull, 2008). Among the last remnants of
forests, the NPEI is one of the most important and it is open for ecotourism. In this
study, it is demonstrated that this activity generates important alterations in the
park’s habitat, supporting our initial hypothesis. An increased number of tourists gen-
erated a significant change in the species composition and a clear decrease in the abun-
dance, biomass, and diversity of the dung beetle assemblage. Therefore the presence of
tourists may negatively affect the structure and ecological functionality of the dry forest
ecosystem.
 JOURNAL OF ECOTOURISM 11

Assemblage structure, bait preferences, and biomass

Tourist presence mainly affected dung beetle abundance. This coincides with the obser-
vations in other studies, in which relatively larger areas and a high degree of disturbance
have been associated with lower beetle abundance (Andresen, 2003; Vidaurre et al., 2008).
It is suggested that this occurs because of a low availability of vertebrate excrement, poss-
ibly induced by ecotourism activity (Lira et al., 2004; Lira & Naranjo, 2003). In general,
beetle assemblage structure was different, in terms of the relative abundance of the domi-
nant species, across the three ecotourism disturbance regimes. This was evident in the
values of the Jaccard index (with a dissimilarity close to 30%), which showed an important
effect in the assemblage structure composition. However, the dominant species between
the three selected sites had a relatively similar value. Therefore, we suggest that the disturb-
ance generated by ecotourism does not directly influence the distribution ranges of the
species that dominate each zone, but does alter their proportions of abundance. For
instance, O. landolti, C. pseudopunticolle, and Uroxys spp. all decrease their abundances
from the LTZ to HTZ; C. femoralis and O. belorhinus, were more abundant in the MTZ
than in the LTZ and their abundance decreased abruptly in the HTZ.
One of the dominant species present throughout the three zones was O. landolti, a
small-size tunneler species with high food preference plasticity. It also uses different
types of dung, has a wide ecological tolerance, and is abundant in tropical and subtropical
areas below 1500 m a.s.l. (Andresen, 2008; Avendaño-Mendoza et al., 2005; Basto-Estrella
et al., 2012; Reyes-Novelo et al., 2007). Another dominant species was C. femoralis, which
is a typical forest species with a wide range of food preferences, being opportunistic as
exhibited by its plasticity in taking advantage of different resources (Estrada & Coates-
Estrada, 2002; Rivera-Cervantes & Halffter, 1999). The high abundance of these species
could indicate a high disturbances regime related to the presence of coffee plantations
and crops in certain zones of the park.
Dung beetle abundances were greater with dung baits than with carrion. This is due to
the fact that most of the species presented coprophagous preferences, which may be
related to a greater availability and quantity of dung in the park, as well as to a greater
degree of spatial aggregation (Cambefort & Hanski, 1991). Another reason could have
to do with the attractiveness of the type of dung used. For instance, Cambefort and
Hanski (1991) mention that some types of dung have a greater capacity of attraction
and detection than others. This may well be the case with human excrement, which
seems to generate a greater attraction than others (Noriega & Fagua, 2009).
Contrary to what was registered for abundance, dung beetle biomass was greater in
carrion than in dung. This can be explained due to the abundance of C. corythus (captured
mainly in carrion), which together with D. centralis (captured in dung), are the species
with the highest biomass in this study. The species D. centralis is highly tolerant to frag-
mentation and loss of habitat and is associated with disturbed zones in the country
(Horgan, 2008). In contrast, C. corythus is considered to be strongly associated with con-
served forest areas (Edmonds & Zidek, 2010). If only biomass is considered, these two
species have a great functional importance for the ecosystem because the amount of
organic matter that they are able to incorporate into the soil is related to the size of the
specimens (Horgan, 2001).
12 J. D. PABLO-CEA ET AL.

Tourism gradient effect and indicator species

The disturbance caused by ecotourism in the park acts as a source of heterogeneity (dis-
similarity in the composition and structure between sites), affecting the dung beetle assem-
blage structure in the three zones. This would explain why although O. landolti presented
the greatest abundance, its presence decreased in higher tourism zones. The relatively
increased disturbance in this zone may have generated a disequilibrium, decreasing the
abundance of this species and generating the opportunity for other species to become
more abundant. Our results contrast with those obtained in different localities in the Neo-
tropical region, where an increase in disturbance was associated with a decrease in even-
ness (Andresen, 2008; Escobar, 1997; Scheffier, 2005). Those studies propose that evenness
decrease could be useful as a potential indicator of the degree of disturbance. Still, the ten-
dency in our study was an increase in evenness as disturbance increased. The results
obtained in this study and others (Noriega et al., 2007; Otavo et al., 2013), could mark
a turning point to question whether this trend should be considered as an efficient indi-
cator of disturbance level or not. It is clear that the sampled sites had low values of even-
ness, showing predominantly the dominance of a species or a group of species, which is
usually recorded as the most frequent structure of dung beetles assemblages (Andresen,
2008; Estrada & Coates-Estrada, 2002).
Field surveys in the Park of the presence of tracks and dung indicated that mammals
have a homogeneous distribution among sites, although they were rarely observed in
the HTZ. This coincides with other studies where sited fauna decreases in places open
to tourism (Lira et al., 2004; Lira & Naranjo, 2003). The White-nosed Coati and the
Nine-banded Armadillo were observed regularly in the zones with tourist access
(Velado-Cano, 2014). The excrement produced by some of these mammals could rep-
resent an important resource for local dung beetles, and especially the omnivorous diet
of the coati which produces potentially more attractive excrement than that produced
by the herbivores (Cambefort & Hanski, 1991). In the case of the armadillo, its diet
could even favor the presence of copro-necrophagous beetles since its dung of mixed
characteristics is composed mostly of the remains of insects, frogs, and reptiles (Davis,
1974). Both species of mammals may also have adapted to the disturbance caused by
tourism in the park, explaining their presence in these areas. This circumstance has
been documented by Hidinger (2007), who recorded that the White-nosed Coati is a
species that is highly adaptable to human presence, even going as far as to beg tourists
for food. Another possible explanation may be that the aforementioned mammalian
species use sites with tourist access as an escape area from predators that prefer to
avoid them (Hidinger, 2007). In the HTZ, a greater number of mammal carcasses were
observed, especially of armadillo. This greater number of dead animals coincides with a
higher frequency of the necrophagous beetle C. corythus, which had the highest abundance
in this site. Although carrion abundance was not quantified in each of the sites, it was
evident that the frequency of mammalian carcasses was higher in the sites with tourist
access than in the conservation zone. This finding is in accordance with one of the
most serious effects of ecotourism, which is an increase in the rate of wild animal mortality
(Knight & Cole, 1995; Wall & Wright, 1977).
In terms of potential indicator species for conserved and perturbed areas, we identified
five species that could be useful in monitoring programs for each of the studied zones.
 JOURNAL OF ECOTOURISM 13

Dichotomius yucatanus is a clear candidate that was associated with disturbed areas and
could be useful to detect high degradation in secondary forests. In contrast,
O. belorhinus and C. femoralis may be good indicators of forest recovery in secondary
forests. Finally, C. pseudopunticolle and P. eximus may be excellent candidate species
for conserved areas, since in this specific scenario, they responded clearly to perturbations
caused by ecotourism. In addition, C. pseudopunticolle constitutes a new record for the
country (Pablo-Cea et al., 2016), indicating a narrow distribution range and a potential
use for future research in the prioritization of conservation areas. Furthermore, it is impor-
tant to mention that in the areas near to the park (less than 20 km of distance) the presence
of the invasive species Euoniticellus intermedius (Reiche, 1849) and Digitonthophagus
gazella (Fabricius, 1787) (Pablo-Cea et al., 2017) have been registered, clearly indicating
an increase in disturbance and degradation pressure of forest areas. In addition, the loss
of three functionally important species (i.e. P. eximus, P. wagneri, and S. mexicanus;
two medium-size tunnelers and one small roller) was correlated with an increase of
tourism, suggesting a reduction in the functional redundancy of the ecosystem. This high-
lights the importance of NPEI as an area that harbors species that have not been found in
other regions of the country. Although in El Salvador there is no official list of dung
beetles, based on the literature and a review of collections, we estimate that there are at
least 53 species of Scarabaeinae reported for the country. The 22 species found in NPEI
(0.19% of the national territory) represent almost 41% of all reported species in the
country, highlighting the importance of the park for maintaining local biodiversity in El
Salvador.
Ecotourism is an activity that could improve the living conditions of local communities,
but must be studied in detail before it is promoted, in order to better predict its potential
negative effects on biodiversity. It is essential to create a culture of ecotourism that encom-
passes its socio-economic significance as well as its contribution to the preservation of
highly diverse areas, as has been accomplished in other parks worldwide (Aylward
et al., 1996; Das & Hussain, 2016; Mathis & Rose, 2016; Rodrigues & Prideaux, 2018; Saur-
ombe et al., 2018). As Boley and Green (2015) point out, it is important that there is a
positive and close ‘symbiotic’ relationship between ecotourism and conservation that
benefits protected areas in addition to having a positive impact on local communities.
In this sense, we recommend performing structured surveys to understand the perception
of the different entities that participate actively in the park’s ecotourism programs with the
objective of an integration of the different perspectives concerning management and
sustainability.

Caveats
It is important to mention that certain site-specific characteristics between localities, such
as agricultural disturbance history, topography, and elevation could have affected our
results, and may even explain some of our dung beetle trends. However, we believe that
these small differences between sites (e.g. less than 200 m of altitude between sites, a differ-
ence of 0.07 in DBH, and a difference of 8% in canopy coverage; see zones and sampling
sites in methods) are not the main cause of the effects that we have observed, and that they
are part of the usual landscape heterogeneity that does not have an effect on dung beetle
diversity (e.g. Andresen, 2008; Davis et al., 1999; Estrada & Coates-Estrada, 2002; Scheffier,
14 J. D. PABLO-CEA ET AL.

2005). Also, we are aware of the absence of a true replication at the treatment level, even
though we tried to compensate for this situation using 20 independent sampling units, in 2
separate transects, and during 6 sampling events. For future studies, it is worthwhile to
compare similar forests with a wider range of tourist intensities in order to have a true
spatial replication.
Our results indicate the occurrence of habitat alterations in the areas with the highest
tourist access. The number of tourists passing through the extensive (MTZ) and intensive
(HTZ) zones influenced the assemblage structure of coprophagous and necrophagous
beetles, potentially affecting the functionality of the ecosystem. However, this negative
effect is not as severe as we initially expected because richness was not strongly altered.
This supports the hypothetical idea that this type of disturbance is in an early phase of
its potential negative impact. From our observations, we believe that the redistribution
of the number of tourists in NPEI between the two paths (HTZ and MTZ) could
reduce the negative impact of ecotourism on dung beetle biodiversity in the HTZ. This
is likely because it is known that ecotourism tends to be less sustainable in mountain
forests in comparison with other types of ecosystems due to the high fragility and low
load capacity of this ecosystem (Krüger, 2005). The most common cause for an ecotourism
project to be considered unsustainable is the excess in the amount of tourists allowed to
access the site, which can exceed a site’s carrying capacity (Krüger, 2005) and generate
a strong negative impact on the environment (Chen, 2015). The use of ecological indi-
cators, especially the implementation of dung beetles as a valid evaluation tool, has
great potential to provide a clearer perspective on the medium and long-term trajectories
of an ecotourism project and its sustainability (Baral, 2015; Buckley, 2003).
To conclude, tourism within NPEI can be characterized as being between the limits of a
simple nature-based tourism and ecotourism (Baral, 2015; Donnelly et al., 2011). It is true
that the ecotourism practice in the Park contributes to the conservation of its biodiversity
and supports tour guides economically, as well as the development of local communities.
However, it is essential to continue to thoroughly evaluate and monitor the ecological
effects of human activity on the environment, with the goal of minimizing its impact as
much as possible. This is the first study to evaluate ecological disturbance of tourist
visits on the Park, an essential requirement for any location that is designated for ecotour-
ism (Baral, 2015; Donnelly et al., 2011). We highlight the necessity to increase these types
of studies and promote the conservation of the last forest remnants that still exist in El
Salvador.

Acknowledgements
We thank Néstor Omar Herrera for the initial suggestion to perform this investigation and MARN
for the scientific collection permission given. We are grateful to Marta Quezada and Enrique
Fuentes of SalvaNatura for the technical and logistic support. We acknowledge Juan Francisco
Pablo for the help in the design of the traps used. We thank the rangers of the park for accompany-
ing in every step of the field investigation. Ángel Solís from the Museo Nacional de Costa Rica is
acknowledged for his valuable help in the identification and confirmation of the species collected.
We are thankful to Víctor Carmona and the Loyola Marymount University for the donation of
equipment used in this study. David Morris, Javier Santos and Hannah James Bowen are acknowl-
edged for kindly checking the English version of the manuscript. JDPC dedicates this work to the
memory of Juan Francisco Pablo.
 JOURNAL OF ECOTOURISM 15

Disclosure statement
No potential conflict of interest was reported by the author(s).

Funding
We are in debt to Juan Francisco Pablo and Ana Virginia Cea for financial support to make this
investigation possible.

ORCID
José D. Pablo-Cea http://orcid.org/0000-0001-5627-835X
Maryory A. Velado-Cano http://orcid.org/0000-0002-0567-4974
Jorge Ari Noriega http://orcid.org/0000-0003-1760-7020

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