504 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

Effects of habitat loss on three insect assemblages in modified ecosystems

of foothills of the Colombian Orinoquia

David Camilo Martínez1,2*., https://orcid.org/0000-0003-0079-558X

Juan E. Carvajal-Cogollo1, https://orcid.org/0000-0002-4542-6967

1. Grupo de Investigación Biodiversidad and Conservación, Museo de Historia Natural Luis Gonzalo Andrade Natural,

Facultad de Ciencias, Universidad Pedagógica y Tecnológica de Colombia, Avenida Central del Norte 39-115, 150003

Tunja, Boyacá, Colombia; martinezd.camilo@gmail.com (*Correspondence), juan.carvajal03@uptc.edu.co

2. Laboratorio de Entomología, Universidad Pedagógica y Tecnológica de Colombia. Tunja, Boyacá, Colombia.

Received 14-I-2022. Corrected 25-IV-2022. Accepted 14-VII-2022.

ABSTRACT

Introduction: The effects of habitat transformation have been widely studied and the effects are well-known at

different levels of biological organization. However, few studies have focused on responses to this process at the

level of multiple taxa in diverse taxonomic and functional groups.

Objective: Determine the variations in taxonomic and functional diversity of ants, butterflies, and dung beetles,

at a spatial and temporal level in a landscape mosaic of the ecoregion of the Colombian foothills.

Methods: We assessed amount of natural habitat and landscape composition in four types of vegetation, during

the highest and lowest rain periods. We collected butterflies with hand nets and used baited pitfall traps for dung

beetles and ants.

Results: Habitat loss positively affected ant and butterfly species richness, and negatively affected dung beetles.

The abundance of ants and butterflies had a positive effect on the dominance of species in the transformed veg-

etation, for dung beetles the abundance was negatively affected by the absence of canopy cover. Habitat loss had

no negative effect on functional diversity as there is no difference between natural and transformed vegetation.

Conclusions: The amount of habitat, habitat connectivity and different types of vegetation cover were impor-

tant factors in the maintenance of insect diversity in the modified ecosystems of foothills of the Colombian

Orinoquia. The lack of a common spatial and temporal pattern shows that studies of multiple insect taxa should

be carried out for biodiversity monitoring and conservation processes.

Key words: habitat fragmentation; habitat amount; ants; butterflies; dung beetles; neotropical landscape.

https://doi.org/10.15517/rev.biol.trop.2022.49628

TERRESTRIAL ECOLOGY

Habitat loss is the process by which natu-

ral vegetation is transformed by anthropogenic

activities into any other type of land use such

as crops, livestock, or urban growth (Collin-

ge, 2009; Fahrig, 2019). These changes have

negative effects on biodiversity, as seen by the

decrease in the number of species, the reduc-

tion in their abundances, and by variations in

the distribution of populations (Fahrig, 2003;

Horváth et al., 2019). In extreme cases where

the amount of natural vegetation remaining in

a landscape is not suitable to support a popu-

lation or assemblage (threshold habitat level)

and the process of habitat loss increases over

time, species extinction may occur (Collinge,

2009; Fahrig, 2001; Sardanyés et al., 2019).

Thus, in landscapes with high levels of trans-

formation, environmental parameters change in

short periods of time, which is more noticeable

in small patches of habitat (hyperdynamism)

505

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

(Laurance, 2002). Even so, the real impact of

habitat loss on biodiversity seems to depend

on the intensity, extent, and type of change in

the vegetation (Arroyo-Rodríguez et al., 2019).

Recently, the global decline and increased

pressures on biodiversity have been widely dis-

cussed (Arroyo-Rodríguez et al., 2019; Fahrig,

2019). It is evident that the decrease in bio-

diversity due to habitat loss is represented

not only by the reduction of species richness

(Macdonald et al. 2020), but also by changes in

climate regulation, the supply of fertile soil and

drinking water, erosion control, and food pro-

duction (Skogen et al., 2018). Insects are not

immune to the effects caused by the decrease

of the habitats they occupy and functional loss

of their communities, decrease in total biomass

and reduction in the number of species, both of

those that are specialists for a type of habitat,

as well as those with wide distributions and

abundant populations, have been documented.

(Forister et al., 2019; Wagner, 2020). The main

factors for the decline of insect assemblages

have been quantified, from the greatest to the

least impact and they are the loss and degrada-

tion of ecosystems, the excessive use of pesti-

cides, and climate change (Jactel et al., 2021;

Sánchez-Bayo & Wyckhuys, 2019). Other fac-

tors include disease, competition with invasive

species, and light pollution caused by urbaniza-

tion (Langevelde et al., 2018). As a result of the

above, the main concerns regarding the decline

of insects are focused on the loss of ecosystem

services they provide such as cycling of organic

matter (decomposition of wood, leaves, manure

and carrion), pest control (arthropods, fungi

and weeds), wildlife nutrition (primary base in

trophic chains), and the main one, pollination

(Forister et al., 2019; Losey & Vaughan, 2006;

Noriega et al., 2018).

Although the effects of habitat transfor-

mation on response variables of communities

such as alpha, beta, and gamma diversity have

been widely studied (Arroyo-Rodríguez et al.,

2019), studies that evaluate the responses of

multiple taxa with contrasting ecological roles

and habitat specializations in tropical forests

are still very few (Filgueiras et al., 2019a). In

addition to the above, studies focused on a sin-

gle taxon may provide incomplete and less use-

ful information for conservation plans, since

the species differ in their sensitivity to habitat

modification and so there are different respon-

ses in life cycle traits, such as dispersal capa-

city, reproductive potential and niche width

(Díaz-García et al., 2020; Kellner et al., 2019).

A multitaxon approach will be of great help for

assessing with greater precision the patterns of

biodiversity loss and the environmental factors

that determine the response to these distur-

bances (Decaëns et al., 2018; Püttker et al.,

2020). Such information is of great importance

for understanding the drivers of the impacts

of habitat loss (Carrié et al., 2017; Filguei-

ras et al., 2019a). Studies including traits at

the functional level are few, even though the

negative effects describing functional impo-

verishment of assemblages and the sensitivity

of functional traits to habitat alteration are

known (Ewers & Didham, 2006; Filgueiras

et al. 2019a). Thus, research that studies the

congruence of taxonomic and functional diver-

sity together will improve our understanding

of biodiversity patterns, the use of resources

in ecosystems, habitat requirements of species,

and environmental factors that function as fil-

ters (Castro et al., 2020; Nunes et al., 2016).

Insects are important components of bio-

diversity and in most terrestrial and aquatic

ecosystems they are the most diverse group,

both taxonomically and functionally (Parikh et

al., 2020; Stork, 2018). We focus on the eva-

luation of the assemblages of three insect taxa:

ants (Hymenoptera: Formicidae), dung beetles

(Coleoptera: Scarabaeinae), and diurnal butter-

flies (Lepidoptera), groups that are traditionally

used for the estimation of diversity, since they

provide reliable information on the conserva-

tion status of a habitat (Andrade-C. et al., 2017;

Fernández et al., 2019; Filgueiras et al. 2019a;

Villarreal et al., 2006). These groups meet the

criteria as good indicators of diversity and

ecological processes: well-known and stable

taxonomy, widely documented natural history,

abundant species that are easy to observe and

manipulate (little sampling effort), lower taxa

506 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

(species and subspecies) with habitat specifici-

ty, sensitivity to changes, and high taxonomic

and ecological diversity (Hayes et al., 2009;

Parikh et al., 2020; Spector, 2006).

We compared the abundance, species rich-

ness and composition of three assemblages of

insects (ants, dung beetles and diurnal but-

terflies) in a landscape mosaic that included

fragments of secondary forest, riparian forests,

pine plantations, and wooded pastures, in the

foothills ecoregion to the east of the Eastern

Cordillera of Colombia. Our objective was to

determine variations in the diversity of species

at the taxonomic and functional level, and

their relationship to the number of available

habitats and seasonal variation during the year

(higher and lower rainfall). We started with the

hypotheses that (1) In line with the documented

importance of forest covers for the conservation

of biodiversity, the highest values of taxonomic

and functional diversity of assemblages will

occur in secondary forests, followed by riparian

forests, and finally plantations and wooded

pastures; (2) the abundance values of the spe-

cies assemblage in plantations and pastures will

differ significantly from those in habitats with

greater forest cover; (3) there will be marked

variations between the periods of higher and

lower rainfall in terms of the richness, compo-

sition and structure of the assemblages of dung

beetles, butterflies and ants; and (4) the amount

of habitat will positively influence the richness

and abundance values, and these will be inde-

pendent of the functional diversity values of the

studied assemblages.

MATERIALS AND METHODS

Study area: This research was carried out

in the foothills ecoregion, in the municipality

of Villavicencio, East of the Eastern Cordillera

of the Colombian Andes (4º8’34.588” S &

73º39’57.805” W), 723-774 m.a.s.l (Fig. 1).

This ecoregion is considered as a transition

Fig. 1. Location of the sampling area in the ecoregion of the Colombian foothills, in the municipality of Villavicencio (Meta).

The 2 000 m diameter circular buffer area centered on the sampling site is shown.

507

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

between the Andean life regions and the high

plains of the Orinoquia region (Carvajal et al.,

2007). The foothills are recognized as a center

of endemism for fauna, called “Refugio de

Villavicencio” (Brown, 1982; Romero et al.,

2004) that extends along the lower slopes (the

foothills) of the Eastern slope of the Eastern

Cordillera in the Colombian Andes (Hernández

et al., 1992). The annual temperature ranges

between 24-32 °C, with precipitation between

24.2-84 mm per year, with minimums between

the months of December and March and maxi-

mums between April and July (Minorta-C. &

Rangel-Ch., 2015). Although the foothills are

considered an ecoregion of high biodiversity

(Rangel-Ch. 2014), its forests are in critical

danger as they have only 16 % of their natural

vegetation intact, 4 % semi-natural vegetation,

and 80 % has been transformed (Etter et al.,

2017; Latorre et al., 2014). The main activities

of transformation and loss of habitat are of

anthropic origin, such as large-scale agricul-

tural crops (silvopastoral systems and mono-

cultures), extensive livestock, illicit crops, and

rapid urban growth (Hernández et al., 2021;

Velosa et al., 2018).

We selected four types of vegetation for

sampling:

Secondary forest (SF): tree cover with a

discontinuous canopy and with a height grea-

ter than 15 m, where the most abundant spe-

cies were Clusia lineata (Clusiaceae), Miconia

serrulata (Melastomataceae) and Phyllanthus

attenuatus (Phyllanthaceae).

Riparian forest (RF): tree cover located

on the margins of running water, no more

than 50 m wide and with a high abundance of

tree species such as Acalypha aff. diversifolia

(Euphorbiaceae), Duroia hirsuta (Rubiaceae),

Miconia serrulata (Melastomataceae) and

Henriettella aff. seemannii (Melastomataceae).

Wooded pasture (WP): dominated by

Poaceae species, with dominance of Panicum

pilosum (Poaceae), Cyperus laxus (Cypera-

ceae) and Andropogon bicornis (Poaceae), in

addition to the presence of the tree Vismia aff.

lauriformis (Hypericaceae).

Pine plantation (PP): monoculture con-

sisting of Pinus patula (Pinaceae) and emerging

species such as Aphelandra pilosa (Acantha-

ceae), Tapirira aff. guianensis (Anacardia-

ceae), Philodendron sp. (Araceae), Costus aff.

spiralis (Costaceae) and Alchornea glandulosa

(Euphorbiaceae). Pastures and pine plantations

represent the most common anthropic pressu-

res on the foothills ecosystems (Rangel-Ch. &

Minorta-C., 2015).

Insect sampling: We carried out six sam-

pling events, three during the season of greater

precipitation in the months of May, June and

July 2019, and three during the season of less

precipitation in March, August and October of

this same year (categories given according to

the precipitation averages given by Minorta-C.

& Rangel-Ch., 2015). During each sampling

event we collected data on the assemblages

of ants, dung beetles, and butterflies. For ants

and dung beetles we used a baited pitfall trap

design, while for butterflies we used nets

standardized by hours/person, replicated in the

landscape with spatial independence. We pla-

ced each set of pitfall traps 30 m away from the

physical border of the fragment for the forest

covers (Dröse et al., 2019; Martínez-Falcón

et al., 2018), and away from the influence of

forests or riparian vegetation by at least 100 m

from wooded pasture and pine plantation (Da

Silva & Hernández, 2015; Dröse et al., 2019).

Specifically, for each taxonomic group we

followed the following protocols: for ants, we

arranged three pitfall traps linearly and baited

with tuna for each vegetation type, separated

from each other by at least 60 m. Each of

the traps was active for 48 hours in each of

the sampling events, giving a total effort of

3 456 h/trap for the six sampling events; each

trap was our sampling unit. For dung beetles

we installed six pitfall traps in a straight line

separated from each other by at least 30 m in

each of the vegetation type; each trap was our

sampling unit. Three traps were baited with

508 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

approximately 30 g of human excrement and

the other three with decomposing fish (Cultid

et al., 2012). We checked and rebaited each of

the traps every 12 hours, and they were kept

active for 72 hours (Villarreal et al., 2006). This

resulted in a sampling effort of 10 368 hours/

trap for the six sampling events. For butterflies

we used two methods for recollection of indivi-

duals. The first was the free search collection

method with an insect nets (Andrade-C. et al.,

2013). In each search we toured and collected

the butterfly individuals that were perched on

the vegetation or active in flight (Andrade-C.

et al., 2013), with a total sampling effort of

2 hours/person/vegetation, in each of the six

sampling events, and total 48 hours/person

for the six sampling events; each hour was

our sampling unit. The second method for

collecting butterflies was the installation of

two Van Someren-Rydon traps in each of the

vegetation types, separated by at least 50 m

from each other, one baited with decomposing

fruit (banana, pineapple, mango, papaya and

beer) and the other with pieces of decomposing

fish (Andrade-C. et al., 2013). Each trap had an

activation time of 48 hours and checked every

12 hours (DeVries, 1987). Thus, a sampling

effort of 2 304 hours/trap was obtained for the

six sampling events.

Ants and beetles collected from each trap

were transported in hermetically sealed bags

and preserved in 70 % alcohol for subsequent

taxonomic determination (Fernández et al.,

2019; Villarreal et al., 2006), and in envelopes

for butterflies (Andrade-C. et al., 2013). The

determination of ants was done following the

keys for subfamily and genera of the book Intro-

duction to the Ants of the Neotropical Region

(Fernández, 2003) and Ants from Colombia

(Fernández et al., 2019); the taxonomic update

of the subfamilies and genera was done through

the revision of the page: http://www.antweb.

org (AntWeb, 2019). For the determination of

dung beetles, the specialized keys were used:

Edmonds & Zídek (2012), Génier (1998),

Génier & Kohlmann (2003), Medina & Lopera-

Toro (2000), Sarmiento-Garcés & Amat-García

(2014) and Vaz de Mello et al. (2011). Butterfly

determination was done with the help of the

Lamas (2004) guide for neotropical butterflies

and the illustrated list of butterflies of the Ame-

ricas by Warren et al. (2017). The biological

material is deposited in the insect collection

of the Luis Gonzalo Andrade Natural His-

tory Museum. Collecting permits are from the

Pedagogical and Technological University of

Colombia, issued by the National Environmen-

tal Licensing Authority of Colombia.

Landscape metrics: We selected two

landscape metrics to assess their influence on

the species richness and functional diversity of

the three groups of insects, (1) the amount of

habitat and (2) the composition of the landsca-

pe (Collinge, 2009; Fahrig, 2013). The amount

in hectares (ha) of each of the vegetation type

is measured in a circular buffer area of 2 000 m

diameter, based on the local landscape concept

provided by Fahrig (2013). According to Fahrig

(2013), the appropriate scale to test the habitat

quantity hypothesis is the scale related to the

average movement ranges of the study species.

Following the previous idea, the buffer was

selected taking into account dispersal studies

of coprophagous beetles (Cultid-Medina et al.,

2015) and butterflies (Marquez & Martínez,

2020) where they describe that the individuals

of these groups can move up to 1.7 km and

1.3 km, respectively. Thus, the 2 km buffer

was selected taking into account the greatest

degree of dispersal of the groups, in this case,

dung beetles. Landscape composition, defined

as the types of habitats or vegetation present in

the landscape (Collinge, 2009), was obtained

according to the standardized Corine Land

Cover methodology (IDEAM et al., 2011). The

Corine Land Cover (CLC) methodology was

born in Europe on june 27, of 1985, with the

start of the CORINE program, “Coordination of

Environmental Information”, which is an expe-

rimental type project that allows describing,

characterizing, classifying and comparing land

cover characteristics, interpreted from the use

of medium resolution satellite images (Land-

sat), for the construction of land cover maps

at different scales (Suárez-Parra et al., 2016).

509

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

These quantities were obtained through the

ArcGIS v. 10.6 (ESRI, 2016) through landsat

images using the GloVis system (USGS, 2019).

Data analysis. Taxonomic diversity: We

used two measures to evaluate alpha diversity,

both based on the effective number of species

from the transformation of qD: diversity of

order zero (q= 0) which is equivalent to the

number of species and diversity of order one

(q= 1), where the weight of each of the species

is proportional to its abundance in the sample

(Jost, 2006). The completeness of the sample

was determined by calculating the coverage

deficit using the bootstrap method with 95

% confidence intervals for interpolation and

extrapolation (Chao & Jost, 2012). To graphi-

cally describe the abundance patterns of insect

taxa in the vegetation types, we calculated

range abundance curves with adjustment for

undetected diversity (Chao et al. 2015). Howe-

ver, we would like to clarify that in the case of

butterflies, we only used the records obtained

from the insect net and omitted the individuals

collected with Van Someren Rydon traps. This

is due to the low number of individuals collec-

ted with the traps and to the fact that these

species had already been recorded with the net

method. For the development of the analyses,

we used the R program (R Core Team, 2019)

and the iNEXT packages for alpha diversity

based on the effective number of species (Hsieh

et al., 2016) and for the abundance range cur-

ves we followed Chao et al. (2015).

Assessment spatial and temporal change

of the insect assemblages: We analyzed the

degree of differentiation of the three groups of

insects among the plant covers and seasons by

calculating the Sorensen dissimilarity (βsor)

and its replacement components (Simpson dis-

similarity index, βsim) and nesting (βnes)

(Baselga, 2010; Baselga, 2012). The exchange

implies the substitution of species between

sites or seasons mainly because of environ-

mental limitations, while nesting implies that

sites poor in species are actually subsets of

sites or periods with greater richness (Baselga,

2010; Baselga, 2012). The differences between

vegetation types and seasons were estimated by

means of the non-parametric analysis of simi-

larity ANOSIM (analysis of similarity of the

abundance matrix) (Clarke & Warwick, 2001).

We developed the analyses in the R program (R

Core Team, 2019), using the betapart (Baselga

et al., 2018) and Vegan for the ANOSIM analy-

ses (Oksanen et al., 2019)

Functional diversity: For ants and dung

beetles we used the ethological functional trait

of food habits. The eating habits of ants were

taken from Fernández (2003) and Fernández

et al. (2019), where a species is a specialist if

it feeds on a single resource, or a generalist if

its feeding habits include both plant material

and arthropods. We categorized dung beetle

species as specialists if more than 70 % of

the individuals were collected by means of a

single type of bait and generalists if there was

no difference between baits (Andresen, 2005).

For butterflies we used and adapted habitat to

categorize them as generalists (species with

preference for non-forest matrices) or specia-

lists (forest-dependent species), according to

Filgueiras et al., (2019b). Thus, the butterfly

species collected in open habitats, transformed

habitats (wooded pasture and pine plantation)

or natural habitats and transformed habitats all

the same time, were categorized as generalists

and the species captured in natural forest covers

(riparian forest secondary forest) were catego-

rized as specialists.

We evaluated functional diversity from

a single-trait approach, through the indices

of Functional Regularity (FRO) and multiple

Functional Divergence (FDvar) (Mason et al.,

2005; Pla et al., 2012). FRO is used to examine

the extent to which effective use is made of the

full range of resources available in each niche

(Mason et al., 2005; Pla et al., 2012). FDvar

is a measure of functional similarity between

the dominant species of an assemblage, where

a high value indicates a high niche differentia-

tion between species, potentially reflecting low

competition and a more efficient distribution

and use of available resources (Córdova-Tapia

510 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

& Zambrano, 2015; Mason et al., 2005). We

did these analyses with the FDivesity software

(Casanoves et al. 2010), with extension to the

R platform (R Core Team, 2019).

Landscape metrics vs taxonomic and

functional diversity: To evaluate the effect of

the amount of habitat and the type of vegetation

on the richness and functional diversity of each

group of insects, we performed a generalized

linear model (GLM) with a Poisson error distri-

bution for the q0 index. To observe if our model

Y ~ amount habitat + vegetation (%) describes

our response variable more than by chance, it

was contrasted with a null model that repre-

sents the absence of some type of effect for the

predictor variable (MacKenzie et al., 2018).

Additionally, we performed a canonical corres-

pondence analysis (CCA), where we compared

a matrix of the response variables (richness of

each taxon) and another with the explanatory

variables (amount of coverage). To evaluate the

significance of the CCA we performed a Wilk’s

Lambda test with 999 permutations. We did

these analyses in the R program (R Core Team,

2019) through the CCA package (González &

Déjean, 2021).

RESULTS

We recorded 17 126 ants, distributed in

eight subfamilies, 35 genera and 75 species/

morphospecies. The subfamily with the hig-

hest species richness was Myrmicinae, which

together with Formicinae, group 73 % of the

taxa found for ants. The most diverse genera

were Camponotus and Pheidole with eight and

seven morphospecies, respectively. For dung

beetles we obtained records of 1 540 indivi-

duals, belonging to nine genera and 24 species/

morphospecies. The most diverse genera were

Deltochilum and Dichotomius with five and

four species, respectively. For butterflies we

registered 309 individuals belonging to six

families, 80 genera and 117 species/morphos-

pecies. The family with the highest number of

species were Nymphalidae and Hesperiidae,

which together accounted for 68 % of the

species found. The most diverse genera were

Heliconius and Mesosemia with six and five

species, respectively.

The rarefaction-extrapolation estimators

showed high sampling coverage for ants and

dung beetles, which means that a high per-

centage of the species of these two groups

present in the assemblages are represented in

the sample, while for butterflies there was a

low completeness. In this way, the ants had a

coverage of 99 % for all the vegetation types.

For dung beetles the representativeness ranged

from 92 % in the wooded pasture to 98-99 %

in the other vegetation types. For butterflies,

the highest representation was in riparian forest

and wooded pasture, both with 66 %, followed

by secondary forest with 63 %, and pine plan-

tation with 50 % (Table 1).

Taxonomic diversity: Ant species rich-

ness (q= 0) was higher in the transformed

vegetation (pine plantation and wooded pas-

ture) and lower in the conserved vegetation

(secondary forest and riparian forest) (Table 1).

When relative abundance was included in the

diversity metric (q= 1), the same pattern was

observed for the richness of species where the

transformed vegetation was more diverse with

the highest values of the effective number of

abundant species (Table 1). Dung beetles had

the highest richness (q= 0) in pine plantation

and riparian forest, followed by secondary

forest; and the wooded pasture had the lowest

number of species. When considering the rela-

tive abundance (q= 1) the pine plantation shows

a higher diversity, with the highest values of the

effective number of abundant species, while the

lowest values were in wooded pasture (Table

1). For butterflies, the wooded pastures and

riparian forest were the vegetation types with

the highest species richness (q= 0), and the

secondary forest had the lowest number of spe-

cies. Despite the above, when considering the

relative abundances (q= 1), the vegetation types

with the highest values of the effective number

of abundant species were pine plantation and

riparian forest (Table 1).

511

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

In general, the three groups had a hierar-

chical order of abundance with a few domi-

nant species that changed between the plant

covers, and many were represented by only a

few individuals (Fig. 2). For ants, we showed a

high dominance of Ochetomyrmex neopolitus

(Fernández, 2003) and Crematogaster tenuicu-

la (Forel, 1904) in riparian forest and wooded

pasture. This second species was the most

dominant in the pine plantation. In the secon-

dary forest, Ochetomyrmex semipolitus (Mayr,

1878) and Crematogaster limata (Smith, 1858)

were the most abundant, followed by Oche-

tomyrmex neopolitus and Crematogaster tenui-

cula. According to the analysis of imperfect

detection of the abundance range curves, it was

expected that 14, 8, 11 and 17 species of low

abundances still remained to be recorded in the

riparian forest, secondary forest, pine planta-

tion and wooded pasture, respectively (Fig. 2).

For dung beetles a dominance of Del-

tochilum (Deltohyboma) sp. 1 was found in

all vegetation types. In riparian forest we

found Onthophagus gr. clypeatus and Eurys-

ternus caribaeus (Herbst, 1789), in secondary

forest Eurysternus caribaeus, and Phanaeus

cambeforti (Arnaud, 1982) was found in pine

plantations. Imperfect detection analyses

showed that three more species can still be

recorded for riparian forest and secondary

forest, four for pine plantation, and eight for

wooded pasture, all with low abundances (Fig.

2). For butterflies, the most abundant species in

each of the vegetation types were different. For

riparian forest Napeogenes inachia johnsoni

(Fox & Real, 1971) had the highest abundance,

followed by species such as Hyposcada illi-

nissa sinilia (Herrich-Schäffer, 1865), Oleria

gunilla lubilerda (Haensch, 1905), Pterony-

mia sp. 1 and Posttaygetis penela (Cramer,

1777). For secondary forest the most abundant

species was Oleria gunilla lubilerda and for

pine plantations it was Mesosemia walteri

(Brévignon, 1998), and for wooded pasture it

was Hermeuptychia hermes (Fabricius, 1775).

The number of species represented by a single

species (singletons) was high in all vegetation

types. For the secondary forest 69 % of the

species had only one individual in the sample,

for wooded pasture 70 %, for riparian forest 72

%, and for pine plantation 74 %. Based on the

imperfect detection analysis, 31 species were

TABLE 1

Alpha diversity for each of the insects assemblages in sectors of foothills, Colombian Orinoquia

Taxa Estimators SF RF WP PP

Ants Q0 37 31 40 41

Q1 7.827 7.649 8.670 11.811

Abundance 2 345 1 271 7 035 2 616

Sample coverage 0.9957 0.9929 0.9986 0.9962

Deficit 0.0043 0.0071 0.0014 0.0038

Dung beetles Q0 14 16 9 16

Q1 4.020 4.037 3.593 4.242

Abundance 329 620 48 553

Sample coverage 0.9879 0.9952 0.9175 0.9928

Deficit 0.0121 0.0048 0.0825 0.0072

Butterflies Q0 32 46 47 39

Q1 22.306 31.150 26.728 31.903

Abundance 59 96 96 58

Sample coverage 0.6300 0.6567 0.6578 0.5042

Deficit 0.3700 0.3433 0.3422 0.4958

SF: secondary forest, RF: riparian forest, WP: wooded pasture, PP: pine plantation.

512 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

Fig. 2. Range abundance curves with probability of detection of the three assemblages of insects. The gray color reflects the species detected, while the black color reflects the species

that are expected to be detected with increasing sampling effort. Riparian forest (RF), secondary forest (SF), wooded pasture (WP) and pine plantation (PP).

513

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

expected with low abundances that still need to

be registered for secondary forest and for woo-

ded pasture 42 are to be expected, for riparian

forest 50 species, and for pine plantation 53

species (Fig. 2).

Spatial Assessment and temporal chan-

ge of the insect assemblages: At the spatial

and temporal level, the change in species

composition was greater for butterflies than

for ants and dung beetles (Fig. 3A, Fig. 3B).

Among the plant covers, the assemblages of

dung beetles (R= 0.389, P= 0.001) and of

ants (R= 0.123, P= 0.003) was statistically

different, while the composition for butterflies

(R= 0.917, P= 0.413) did not have statistically

significant differences. When considering the

components of beta diversity for the three

groups, the process that best explains the

compositional changes between plant covers is

species turnover (βsim), to a lesser extent for

dung beetles than for ants and butterflies (Fig.

3C). Similarly, species composition changes

between seasons were explained by species

turnover (βsim) rather than by nesting (βnes)

(Fig. 3D). However, there were no statistically

significant differences among the assemblages,

between the high and low rainfall season: ants

(R= 0.083, P = 0.271), dung beetles (R= -0.115,

P = 0.496) and butterflies (R= -0.374, P = 1).

Functional diversity: Functional regu-

larity (FRO) showed differential behavior in

each of the insect groups. For ants, the values

Fig. 3. Spatial and temporal beta diversity for insect assemblages: a. Spatial beta (βsor) diversity. b. Temporal beta (βsor)

diversity. c. Percentage contribution of turnover (dark gray) and nesting (light gray) to spatial beta diversity. d. Percentage

contribution of turnover (dark gray) and nesting (light gray) to temporal beta diversity.

514 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

were the same in all vegetation types. For dung

beetles, the lowest values were in riparian forest

and pine plantation, while the highest value was

in wooded pasture. For butterflies, the wooded

pasture had the lowest value, followed by ripa-

rian forest, and the secondary forest and the

pine plantation had the same value (Table 2).

Similarly, functional divergence (FDvar) had

differential responses for the three groups in

each vegetation type (Table 2). For ants, it had

its highest values in riparian forest and secon-

dary forest, while the lowest value was in pine

plantation (Table 2). In dung beetles, the pine

plantation and the secondary forest had the

highest values, while the riparian forest had the

lowest value. Finally, for butterflies, the secon-

dary forest had the highest value, followed by

the pine plantation, while the riparian forest

and the wooded pasture had the lowest values.

Landscapes metrics vs taxonomic

and functional diversity: Species richness

and functional regularity showed a signifi-

cant relationship with the amount of habitat,

P = 0.0444 and P = 0.0442, respectively. While

the functional divergence did not have statis-

tically relationship with the amount of habitat

(P= 0.0426) (Table 3). The total variance of the

richness explained by the amount of habitat and

vegetation type was 14 % (inertia) according to

the CCA. In addition to the above, each assem-

bly showed a significant relationship with the

different variables (Wilk’s Lambda= 0.2613, F=

0.6456, P= 0.0010). Thus, the richness of dung

beetles had a significant relationship with the

riparian forest and pine plantation, the richness

of butterflies with the open pasture and the rich-

ness of ants with the secondary forest (Fig. 4).

DISCUSSION

Taxonomic and functional diversity:

Contradicting our hypothesis, the natural forest

covers of riparian forest and secondary forest

did not have differential effects on species rich-

ness compared to pine plantation and wooded

pasture. For insects, responses to habitat loss

can be positive when there is evidence of an

accumulation of individuals and intraspeci-

fic aggregation in fragments, or they can be

TABLE 3

Results of the generalized linear model and the null model

Response variable Model AIC ΔAIC ωi

Richness ~Amount 1 416.3 0.00 0.726

~Null 1 418.3 1.95 0.274

FRO ~Amount -952.8 0.00 0.738

~Null -950.7 2.07 0.262

FDvar ~Amount -473.9 1.36 0.336

~Null -475.2 0.00 0.664

The Akaike information criterion (AIC) is shown, the difference between AIC of each model (ΔAIC) and the Akaike weight

(ωi).

TABLE 2

Functional regularity (FRO) and functional divergence (FDvar) for the three groups of insects in each of

the plant covers: riparian forest (RF), secondary forest (SF), pine plantation (PP) and wooded pasture (WP)

Taxa FRO FDvar

RF SF PP WP RF SF PP WP

Ants 0.03 0.03 0.03 0.03 0.34 0.34 0.07 0.32

Dung beetles 0.07 0.08 0.07 0.13 0.11 0.21 0.25 0.16

Butterflies 0.02 0.03 0.03 0 0.2 0.31 0.23 0

515

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

negative when responses are associated with

an increase in rare species (Crist et al., 2006;

Davies et al., 2004). In accordance with the

above and in a general way, the loss of habitat

positively affected the species richness of ants

and butterflies and negatively affected the dung

beetles. On the other hand, the abundance of

the ant and butterfly assemblages was positi-

vely affected by the loss of habitat by showing a

high dominance of a few species that increased

the abundance of individuals in the transformed

vegetation, while for dung beetles the abun-

dance of individuals was negatively affected in

the wooded pasture and positively in the pine

plantation. Ants and butterflies were congruent

in the effects of habitat loss, while beetles had

a differential response.

The high richness and abundance of domi-

nant ant species in pine plantation and wooded

pasture could be associated with the fact that

these species belong to subfamilies of genera-

list habits such as Myrmicinae, Dolichoderinae

and Formicinae, which can exploit a great

diversity of microhabitats and resources by

having superior colonization capacity (Cuezzo,

2003; Fernández et al., 2019). In this way, these

generalist species may be displacing specialist

species, since they have a greater tolerance to

extreme conditions and are more efficient in

the use of the remaining resources as a conse-

quences of habitat loss (Sanabria-Blandón & de

Ulloa, 2011). The simplification of ant assem-

blages due to habitat loss has been documented

previously (Dias et al., 2008; González et al.,

2018). However, the presence of monocultures

and trees in pastures, can provide greater habi-

tat heterogeneity and, therefore, an increase in

the number of species, due to an increase in

feeding sites and nesting sites (Bernardes et

al., 2020; Dias et al., 2008; Rivera et al., 2008).

This may also be a consequence of the microen-

vironmental similarities of wooded pastures

with native vegetation, meaning that the vege-

tation structure in wooded pastures may supply

the requirements of ant assemblages (Queiroz

et al., 2020). In addition, the high diversity of

Fig. 4. Canonical correspondence analysis (ACC) between amount of habitat, amount of border, type of habitat, and richness

of insects. RF (riparian forest), SF (secondary forest), PP (pine plantation), WP (wooded pasture).

516 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

ant assemblages, may also be determined by

the distance to native habitats, which may drive

the high richness values in transformed habitats

(Queiroz & Ribas, 2016; Queiroz et al., 2020).

Dung beetles showed greatest richness

and abundance in the canopy covers, inclu-

ding pine plantations, with species richness

and abundance similar to riparian forest and

secondary forest. Patterns where richness and

abundance are greater in canopy plant covers

than in open areas such as pastures is a pattern

previously documented for this group of insects

(Barragán et al., 2011; Davies et al., 2020;

Giménez-Gómez et al., 2018; Scholtz et al.,

2009). These changes in natural vegetation act

as an environmental filter, reducing the diver-

sity of dung beetle communities and causing

changes in species composition (Cardinale et

al., 2012). This pattern may be associated with

the fact that forest vegetation provides bet-

ter microenvironmental conditions than open

areas: a greater supply of food resources due

to a greater presence of fauna, a decrease in

soil temperature, protection against excessive

radiation, and a greater quantity of leaf litter

which provides protection and improves soil

conditions for nesting (Edwards et al., 2017;

Nunes et al., 2018; Senior et al., 2017). This

result shows that conservation of the cano-

py (native or exotic) in the ecosystems is an

important factor in the preservation of an

assemblage of dung beetles of native forests

by improving microenvironmental conditions

and soil quality (Giménez-Gómez et al., 2018;

Gómez-Cifuentes et al., 2020)

As documented, the effect of habitat loss

on butterfly assemblages can be positive and

maintain high diversity rather than poor com-

munities of individuals and low species rich-

ness (Filgueiras et al., 2016; Filgueiras et al.,

2019b; Melo et al., 2019). However, the low

representativeness for this group is demonstra-

ted by the high number of singletons (60 % of

the species) and doubletons (16 % of the spe-

cies) present in the sample. In addition, these

two groups represent 23 % and 12 % of the

total abundance of the sample. This high num-

ber of singletons and doubletons in the sample

has a negative influence on the sampling cove-

rage, so there may be a degree of subsampling

(Cultid-Medina & Escobar, 2019). This shows

the adaptation of some species to disturbances

and modification of natural habitats that pro-

motes a decrease in sensitive species and an

increase in generalist species (Filgueiras et al.,

2019b). Also, the high species richness in the

wooded pasture may be a result of an increase

in pioneer plant species which in turn increases

the availability of floristic resources that serve

as a food source, both for adults and larvae, in

comparison to forest cover (Melo et al., 2019;

Vargas-Zapata et al., 2011).

The spatial turnover of the three groups

in response to changes in the vegetation types

may be associated with environmental and

microhabitat variations that promote a loss

and gain of species (Baselga & Leprieur,

2015; Baselga et al., 2018). These differences

between the natural and transformed vegeta-

tion intensify the environmental filters for the

typical species of natural habitats and allow an

increase of generalist species and rare or highly

sensitive species (Santoandré et al., 2019). This

may explain the absence of differences for ant

assemblages between plant covers, since the

new environmental conditions favor the coloni-

zation of atypical species towards natural habi-

tats from modified environments (Santoandré

et al., 2019). For dung beetles, environmental

filters are also a factor that determines the abs-

ence of differences in composition among the

plant covers; however, the proximity between

natural and transformed vegetation can cause

the riparian forest to be a source of individuals

for recolonization of the transformed vegeta-

tion and consequently, help in the maintenance

of dung beetle diversity (Gilroy & Edwards,

2017). For butterflies, the low abundance of

many species and the high number of rare (uni-

que) species in the wooded pasture may indica-

te that they only use this area as a foraging area

(Debinski & Holt, 2000).

Contrary to what we expected, functional

diversity was low both in natural vegetation

(riparian forest and secondary forest) and in

transformed vegetation (pine plantation and

517

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

wooded pasture) for the three groups of insects.

At the ecosystem level, these low functional

values could cause lower productivity, stability

and resilience in the communities, since resou-

rces are not used in an optimal way due to low

species complementarity (Kinzig et al., 2002;

Mason et al., 2005).

Our results show that habitat loss does not

have negative effects on functional diversity

since there are no differences between natural

and transformed vegetation. It can be assu-

med that the response relationship depends

on various factors. (1) The functional trait

considered: the high number of individuals

of generalist species that we observed may

be masking the true effects of habitat loss on

the functional diversity of the insect species

(Cadotte et al., 2011). Thus, generalist species

that contribute disproportionately to ecosystem

functions have unique functional traits that

allow them to capture more resources avai-

lable in the different plant covers (Mason et

al., 2005; Mouillot et al., 2005). (2) Species

richness does not greatly influence the results

of the functional diversity, so our results show

that there may be a high functional redundancy

in the three groups of insects among the diffe-

rent vegetation types (Filgueiras et al., 2019a;

Pla et al., 2012); consequently, the loss or gain

of species caused by the loss of habitat, can be

compensated due to the existence of functio-

nally similar species (Cadotte et al., 2011). (3)

The high dominance of generalist species over

specialist species greatly affects the functional

diversity of the three groups of insects, as

has already been documented for these three

groups (Filgueiras et al., 2019a). Consequently,

the loss or decline of forest-dependent spe-

cies (i.e., disturbance-sensitive species) can

be offset by the proliferation of disturbance-

adapted species that maintain community-level

attributes (i.e., abundance, species richness) in

tropical landscapes with anthropic intervention

(Filgueiras et al., 2019a). Our results show a

differential response of each insect group with

respect to habitat transformation (quantity and

type). The lack of congruence among the three

insect groups provides information necessary

to support multitaxon studies and for biodi-

versity monitoring, since a single taxon cannot

provide a reliable view of biotic responses

to habitat loss.

Does the amount of habitat affect

the taxonomic and functional diversity of

insects? Species richness and functional regu-

larity were influenced by the amount of habitat

in the study area. Thus, in landscapes where

the level of habitat loss is low, the remnants

of natural vegetation maintain high structural

connectivity and therefore high diversity, con-

tributing to the increase in migratory species

between vegetation types and maintaining com-

munities with high number of species (Fahrig,

2003; Püttker et al., 2011). However, it should

be noted that our results should be interpreted

as a first approach to the effect of the amount

of habitat in this region of foothills, since the

area that was chosen as a sample of the region.

The foregoing may mean that this landscape

metric (amount of habitat) is not the only one

that may be acting on the diversity of insects

and that there are other drivers that contribute

to the richness of insect species, for example,

proximity and composition of the vegetation

in the landscape (Fahrig, 2013; Fahrig et al.,

2019). This agrees with Watling et al. (2020),

who describe the proximity between patches as

one of the most important drivers of richness

in a landscape, and with Fahrig et al. (2019)

who describe low competition, diversity of

habitats in the landscape, and a greater suc-

cess of movement between patches, as factors

that can counteract the negative effects due

to habitat loss.

Similarly, another factor that differentia-

lly influences species richness in each of the

insect assemblages is the composition of the

vegetation, rather than the configuration of the

patches in the landscape (i.e., size, shape, level

of fragmentation) as has been demonstrated

in other taxa (Arroyo-Rodríguez et al., 2016;

Püttker et al., 2020). For example, for ants

and butterflies the wooded pasture is a type

of high-quality matrix that contains resources,

facilitates movement between forest patches

518 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

and buffers the negative effects of the loss of

natural vegetation (Arroyo-Rodríguez et al.,

2020). These shade-using species require less

forest in the landscape to survive, resulting in

an interaction between the amount of habitat

and the quality of the matrix (Fahrig, 2001).

Regarding the dung beetles and their relation-

ship with the riparian forest, this type of cove-

rage is of utmost importance for species that

depend on humid environments for their repro-

duction, by maintaining minimal fluctuations

in environmental conditions and, to a greater

extent, by promoting biological connectivity

between patches when used as biological corri-

dors (Arroyo-Rodríguez et al., 2020; Fischer &

Lindenmayer, 2007).

Our study provides evidence that the

amount of habitat is a factor of great relevance

for the maintenance of diversity in a landscape.

However, habitat connectivity and heterogenei-

ty of a landscape are important factors in the

maintenance of insect diversity, both for spe-

cies that are not very sensitive and for species

highly sensitive to disturbances, as previously

demonstrated in other studies (Filgueiras et

al., 2016; Melo et al., 2019). Finally, we want

to highlight the importance of the remnants of

natural vegetation which function as sources

and biological corridors that maintain patterns

of diversity in the landscape. Thus, efforts at

biodiversity conservation should be aimed at

maintaining and increasing the connectivity of

the landscape by increasing the amount of natu-

ral habitat, for example, through restoration

or regeneration.

Temporaral variation: Although turnover

explains the beta diversity between seasons,

the absence of differences in the composition

may be due to an overlap in the reproducti-

ve seasons of the insect species: cycles with

irregular mortality but with constant repro-

duction (Kishimoto-Yamada & Itioka, 2015).

This suggests that the communities are stable

over time (Sackmann, 2006). These minimal

changes in the composition of insects may be

associated with the low monthly fluctuation

in rainfall regimes that are characteristic of

neotropical areas (Kishimoto-Yamada & Itioka,

2015). However, even though precipitation

is an environmental variable that affects the

dynamics of arthropod communities (Kishi-

moto-Yamada & Itioka, 2015; Mariottini et al.,

2012), the composition and structure of insect

assemblages over time may be influenced by

other variables such as the structure and com-

position of the vegetation (Casas-Pinilla et al.,

2017; Mahecha-Jiménez et al., 2011).

Implications for conservation: Our study

contributes to an understanding of the patterns

caused by habitat loss at the level of composi-

tion, species richness, abundance, and spatial

and temporal change in groups of insects with

different ecological roles in a transformed area

with a deficit of information on biodiversity.

Our results show that for insects, the amount

of habitat and their connectivity, indicated

by the proximity of natural vegetation to the

transformed vegetation, are important factors

for the maintenance of biodiversity in modified

ecosystems of the foothills of Orinoquia. In

addition to the above: (1) the type of pastures

also plays an important role in maintaining the

diversity of insects; that is, the quality of the

matrix plays an important role in ecosystems

with anthropic disturbances (Fahrig, 2001): (2)

natural vegetation patches, which are relatively

small in the landscape, can play an impor-

tant role in maintaining the taxonomic and

functional diversity of insect assemblages in

the region, as has been demonstrated in other

studies (Fahrig, 2017; Fahrig, 2019). In this

way, conservation efforts should be aimed at

restoring landscape connectivity and modifying

transformed ecosystems so that they are more

amenable to biodiversity, such as moving from

clean cattle pastures to wooded pastures.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is

no conflict of interest of any kind; and that

we followed all pertinent ethical and legal

procedures and requirements. All financial

sources are fully and clearly stated in the

519

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

acknowledgements section. A signed document

has been filed in the journal archives.

ACKNOWLEDGMENTS

We thank The Andean Road Consortium

and UPTC for financing this project, María

Isabel Bautista and Diógenes Arrieta from

CONANDINO who collaborated on logistical

aspects in the field trips. Irina Tatiana Morales

Castaño and the team of the UPTC Entomolo-

gy Laboratory for their support. Andrés David

Meneses for their help in ant determinations.

María Paula Chacón Gutierrez for their help

in butterfly determinations. We express our

gratitude to the call 08-2021, and the pro-

ject: “Taxonomic and functional diversity of

coprophagous beetles (Scarabaeidae: Scara-

baeinae) in a gradient altitudinal of the Nor-

theastern Andes, Boyacá-Colombia. SGI 3150”

of the Vicerrectoría de Investigación y Exten-

sión, of the Universidad Pedagógica y Tecno-

lógica de Colombia (UPTC). We also want to

thank the project: “The biodiversity of Boyacá:

Complementation and synthesis through alti-

tudinal gradients and implementations of its

incorporation in projects of social appropria-

tion of knowledge and the effects of climate

change, Boyacá. BPIN 2020000100003”

RESUMEN

Efectos de la pérdida de hábitat en tres ensambles

de insectos en ecosistemas modificados

de Piedemonte en la Orinoquia colombiana

Introducción: Los efectos de la transformación del hábitat

han sido ampliamente estudiados y son bien conocidos los

efectos a diferentes niveles de organización biológica. Sin

embargo, pocos estudios se han centrado en las respuestas

a este proceso a nivel de múltiples taxones en diversos

grupos taxonómicos y funcionales.

Objetivo: Determinar las variaciones en la diversidad taxo-

nómica y funcional de hormigas, mariposas y escarabajos

coprófagos, a nivel espacial y temporal en un mosaico

paisajístico de la ecorregión del piedemonte colombiano.

Métodos: Evaluamos la cantidad de hábitat natural y la

composición del paisaje en cuatro tipos de vegetación,

durante los períodos de mayor y menor lluvia. Recolec-

tamos mariposas con redes de mano y usamos trampas de

caída con cebo para escarabajos coprófagos y hormigas.

Resultados: La pérdida de hábitat afectó positivamente

la riqueza de especies de hormigas y mariposas y afectó

negativamente a los escarabajos peloteros. La abundancia

de hormigas y mariposas tuvo un efecto positivo sobre la

dominancia de especies en la vegetación transformada,

para los escarabajos coprófagos la abundancia se vio afec-

tada negativamente por la ausencia de cobertura de dosel.

La pérdida de hábitat no tuvo un efecto negativo sobre

la diversidad funcional ya que no hay diferencia entre la

vegetación natural y la transformada.

Conclusiones: La cantidad de hábitat, la conectividad del

hábitat y los diferentes tipos de cobertura vegetal fueron

factores importantes en el mantenimiento de la diversidad

de insectos en los ecosistemas modificados del piedemonte

de la Orinoquia colombiana. La falta de un patrón espacial

y temporal común muestra que se deben realizar estudios

de múltiples taxones de insectos para los procesos de moni-

toreo y conservación de la biodiversidad.

Palabras clave: fragmentación del hábitat; cantidad de

hábitat; hormigas; mariposas; escarabajos peloteros; pai-

saje neotropical.

REFERENCES

Andrade-C., M. G., Campos-Salazar, L. R., González-

Montaña, L. A., & Pulido-B., H. P. (2017). Santa

María Mariposas alas y color. Instituto de Ciencias

Naturales, Universidad Nacional de Colombia.

Andrade-C., M. G., Henao Bañol, E. R., & Triviño, P.

(2013). Técnicas y procesamiento para la recolección,

preservación y montaje de mariposas en estudios de

biodiversidad y conservación. (Lepidoptera: Hes-

perioidea - Papilionoidea). Revista de la Academia

Colombiana de Ciencias Exactas, Físicas y Natu-

rales, 37(144), 311–325. https://doi.org/10.18257/

raccefyn.12

Andresen, E. (2005). Effects of season and vegetation type

on community organization of Dung Beetles in a Tro-

pical Dry Forest. Biotropica, 37(2), 291–300. https://

doi.org/10.1111/j.1744-7429.2005.00039.x

AntWeb. (2019). AntWeb (Version 8.75.3). California Aca-

demy of Science. https://www.antweb.org

Arroyo-Rodríguez, V., Arasa-Gisbert, R., Arce-Peña, N.,

Cervantes-López, M. J., Cudney-Valenzuela, S. J.,

Galán-Acedo, C., Hernández-Ruedas, M. A., Rito, K.

F., & San-José, M. (2019). Determinantes de la biodi-

versidad en paisajes antrópicos: Una revisión teórica.

In C. E. Moreno (Ed.), La biodiversidad en un mundo

cambiante: Fundamentos teóricos y metodológicos

para su estudio (pp. 65–111). Universidad Autónoma

del Estado de Hidalgo/Libermex.

Arroyo-Rodríguez, V., Fahrig, L., Tabarelli, M., Watling,

J. I., Tischendorf, L., Benchimol, M., Cazetta, E.,

Faria, D., Leal, I. R., Melo, F. P. L., Morante-Filho,

520 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

J. C., Santos, B. A., Arasa-Gisbert, R., Arce-Peña,

N., Cervantes-López, M. J., Cudney-Valenzuela, S.,

Galán-Acedo, C., San-José, M., Vieira, I. C. G., …

Tscharntke, T. (2020). Designing optimal human-

modified landscapes for forest biodiversity conserva-

tion. Ecology Letters, 23(9), 1404–1420. https://doi.

org/10.1111/ele.13535

Arroyo-Rodríguez, V., Rojas, C., Saldaña-Vázquez, R.

A., & Stoner, K. E. (2016). Landscape composition

is more important than landscape configuration for

phyllostomid bat assemblages in a fragmented biodi-

versity hotspot. Biological Conservation, 198, 84–92.

https://doi.org/10.1016/j.biocon.2016.03.026

Barragán, F., Moreno, C. E., Escobar, F., Halffter, G., &

Navarrete, D. (2011). Negative impacts of human

land use on dung beetle functional diversity. PLoS

ONE, 6(3), e17976. https://doi.org/10.1371/journal.

pone.0017976

Baselga, A. (2010). Partitioning the turnover and nested-

ness components of beta diversity. Global Ecolo-

gy and Biogeography, 19(1), 134–143. https://doi.

org/10.1111/j.1466-8238.2009.00490.x

Baselga, A. (2012). The relationship between species

replacement, dissimilarity derived from nested-

ness, and nestedness. Global Ecology and Bio-

geography, 21(12), 1223–1232. https://doi.

org/10.1111/j.1466-8238.2011.00756.x

Baselga, A., & Leprieur, F. (2015). Comparing methods

to separate components of beta diversity. Methods in

Ecology and Evolution, 6(9), 1069–1079. https://doi.

org/10.1111/2041-210X.12388

Baselga, A., Orme, D., Villeger, S., De Bortoli, J., &

Leprieur, F. (2018). betapart: Partitioning Beta

Diversity into Turnover and Nestedness Components

(R package version 1.5.1). https://cran.r-project.org/

package=betapart

Bernardes, E. J., Rocha, E. C., Jesus, F. G., Oliveira, M. A.,

& Araújo, M. S. (2020). Dry Forest fragmentation in

Brazilian Cerrado and its effects on communities of

Ground foraging ants. Florida Entomologist, 103(3),

384–391. https://doi.org/10.1653/024.103.0311

Brown Jr., K. S. (1982). Paleoecology and regional patterns

of evolution in neotropical forest butterflies. In G. T.

Prance (Ed.), Biological Diversification in the Tropics

(pp. 255–308). Columbia University Press.

Cadotte, M. W., Carscadden, K., & Mirotchnick, N. (2011).

Beyond species: functional diversity and the mainte-

nance of ecological processes and services. Journal

of Applied Ecology, 48(5), 1079–1087. https://doi.

org/10.1111/j.1365-2664.2011.02048.x

Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U.,

Perrings, C., Venail, P., Narwani, A., MacE, G. M.,

Tilman, D., Wardle, D. A., Kinzig, A. P., Daily, G. C.,

Loreau, M., Grace, J. B., Larigauderie, A., Srivastava,

D. S., & Naeem, S. (2012). Biodiversity loss and

its impact on humanity. Nature, 486(7401), 59–67.

https://doi.org/10.1038/nature11148

Carrié, R., Andrieu, E., Cunningham, S. A., Lentini, P.

E., Loreau, M., & Ouin, A. (2017). Relationships

among ecological traits of wild bee communities

along gradients of habitat amount and fragmentation.

Ecography, 40(1), 85–97. https://doi.org/10.1111/

ecog.02632

Carvajal, L., Patarroyo, J., Puentes, D., & Valero, J. (2007).

Caracterización florística y estructural del piedemon-

te llanero en el departamento del Meta. Corporación

para el Desarrollo Sostenible del Área de Manejo

Especial La Macarena (Cormacarena), Universidad

Distrital Francisco José de Caldas, Colombia.

Casanoves, F., Pla, L., Di Rienzo, J. A., & Díaz, S.

(2010). FDiversity: a software package for the inte-

grated analysis of functional diversity. Methods in

Ecology and Evolution, 2(3), 233–237. https://doi.

org/10.1111/j.2041-210X.2010.00082.x

Casas-Pinilla, L. C., Mahecha-J., O., Dumar-R., J. C., &

Rpios-Málaver, I. C. (2017). Diversidad de mariposas

en un paisaje de bosque seco tropical, en la Mesa

de los Santos, Santander, Colombia (Lepidoptera:

Papilionoidea). SHILAP Revista de Lepidopterología,

45(177), 83–108.

Castro, F. S., Da Silva, P. G., Solar, R., Fernandes, G. W., &

Neves, F. S. (2020). Environmental drivers of taxono-

mic and functional diversity of ant communities in a

tropical mountain. Insect Conservation and Diversity,

13(4), 393–403. https://doi.org/10.1111/icad.12415

Chao, A., Hsieh, T. C., Chazdon, R. L., Colwell, R. K.,

Gotelli, N. J., & Inouye, B. D. (2015). Unveiling the

species-rank abundance distribution by generalizing

the Good-Turing sample coverage theory. Ecology,

96(5), 1189–1201. https://doi.org/10.1890/14-0550.1

Chao, A., & Jost, L. (2012). Coverage-based rarefaction

and extrapolation: standardizing samples by comple-

teness rather than size. Ecology, 93(12), 2533–2547.

https://doi.org/10.1890/11-1952.1

Clarke, K. R., & Warwick, R. (2001). Change in marine

communities: an approach to statistical analysis and

interpretation (2nd Ed.). PRIMER-E Ltd.

Collinge, S. K. (2009). Ecology of fragmented landscapes.

Johns Hopkins University Press.

Córdova-Tapia, F., & Zambrano, L. (2015). La diversidad

funcional en la ecología de comunidades. Revista

Ecosistemas, 24(3), 78–87. https://doi.org/10.7818/

RE.2014.24-3.00

Crist, T. O., Pradhan-Devare, S. V., & Summerville, K. S.

(2006). Spatial variation in insect community and

species responses to habitat loss and plant community

521

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

composition. Oecologia, 147(3), 510–521. https://

doi.org/10.1007/s00442-005-0275-1

Cuezzo, F. (2003). Subfamilia Dolichoderinae. In F. Fernán-

dez (Ed.), Introducción a las Hormigas de la Región

Neotropical (p. 398). Instituto de Investigación de

Recursos Biológicos Alexander von Humboldt.

Cultid, C. A., Medina, C. A., Martínez Quintero, B. G.,

Escobar Villa, A. F., Constantino Chuaire, L. M., &

Betancur Posada, N. J. (2012). Escarabajos copró-

fagos (Scarabaeinae) del Eje Cafetero: guía para el

estudio ecológico (1st Ed.). Wildlife Conservation

Society (WCS) Colombia & CENICAFÉ (Federación

Nacional de Cafeteros de Colombia).

Cultid-Medina, C., & Escobar, F. (2019). Pautas para la

estimación y comparación estadística de la diversidad

biológica (qD). In C. E. Moreno (Ed.), La biodiversi-

dad en un mundo cambiante: Fundamentos teóricos

y metodológicos para su estudio (pp. 175–202). Uni-

versidad Autónoma del Estado de Hidalgo/Libermex.

Cultid-Medina, C. A., Martínez-Quintero, B. G., Escobar,

F., & de Ulloa, P. C. (2015). Movement and popu-

lation size of two dung beetle species in an Andean

agricultural landscape dominated by sun-grown

coffee. Journal of Insect Conservation, 19(4), 617–

626. https://doi.org/10.1007/S10841-015-9784-3

Da Silva, P. G., & Hernández, M. (2015). Spatial Patterns

of Movement of Dung Beetle Species in a Tropical

Forest Suggest a New Trap Spacing for Dung Beetle

Biodiversity Studies. PLoS ONE, 10(5), e0126112.

https://doi.org/10.1371/journal.pone.0126112

Davies, R. W., Edwards, D. P., & Edwards, F. A. (2020).

Secondary tropical forests recover dung beet-

le functional diversity and trait composition. Ani-

mal Conservation, 23(5), 617–627. https://doi.

org/10.1111/acv.12584

Davies, K. F., Margules, C. R., & Lawrence, J. F. (2004).

A synergistic effect puts rare, specialized species at

greater risk of extinction. Ecology, 85(1), 265–271.

https://doi.org/10.1890/03-0110

Debinski, D. M., & Holt, R. D. (2000). A survey and

overview of habitat fragmentation experiments.

Conservation Biology, 14(2), 342–355. https://doi.

org/10.1046/j.1523-1739.2000.98081.x

Decaëns, T., Martins, M. B., Feijoo, A., Oszwald, J., Dolé-

dec, S., Mathieu, J., Arnaud de Sartre, X., Bonilla,

D., Brown, G. G., Cuellar Criollo, Y. A., Dubs, F.,

Furtado, I. S., Gond, V., Gordillo, E., Le Clec’h, S.,

Marichal, R., Mitja, D., de Souza, I. M., Praxedes,

C., … Lavelle, P. (2018). Biodiversity loss along a

gradient of deforestation in Amazonian agricultural

landscapes. Conservation Biology, 32(6), 1380–1391.

https://doi.org/10.1111/cobi.13206

DeVries, P. J. (1987). The butterflies of Costa Rica

and their natural history. Papilionidae, Pieridae,

Nymphalidae. Princeton University Press.

Dias, N. S., Zanetti, R., Santos, M. S., Louzada, J., &

Delabie, J. (2008). Interação de fragmentos flo-

restais com agroecossistemas adjacentes de café e

pastagem: Respostas das comunidades de formi-

gas (Hymenoptera, Formicidae). Iheringia - Serie

Zoologia, 98(1), 136–142. https://doi.org/10.1590/

S0073-47212008000100017

Díaz-García, J. M., López-Barrera, F., Pineda, E., Toledo-

Aceves, T., & Andresen, E. (2020). Comparing the

success of active and passive restoration in a tro-

pical cloud forest landscape: A multi-taxa fauna

approach. PLoS ONE, 15(11), e0242020. https://doi.

org/10.1371/journal.pone.0242020

Dröse, W., Podgaiski, L. R., Dias, C. F., & Mendonça,

M. de S. (2019). Local and regional drivers of ant

communities in forest-grassland ecotones in South

Brazil: A taxonomic and phylogenetic approach.

PLoS ONE, 14(4), e0215310. https://doi.org/10.1371/

journal.pone.0215310

Edmonds, W. D. & Zídek, J. (2012). Taxonomy of Pha-

naeus revisited: Revised keys to and comments

on species of the New World dung beetle genus

Phanaeus MacLeay, 1819 (Coleoptera: Scarabaei-

dae: Scarabaeinae: Phanaeini). Insecta Mundi, 0274,

1–108.

Edwards, F. A., Finan, J., Graham, L. K., Larsen, T. H.,

Wilcove, D. S., Hsu, W. W., Chey, V. K., & Hamer,

K. C. (2017). The impact of logging roads on dung

beetle assemblages in a tropical rainforest reserve.

Biological Conservation, 205, 85–92. https://doi.

org/10.1016/j.biocon.2016.11.011

ESRI. (2016). ArcGIS (Version 10.6). Environmental Sys-

tems Research Institute. https://www.esri.com/en-us/

arcgis/products/arcgis-pro/overview.

Etter, A., Angela, A., Saavedra, K., Amaya, P., Arevalo, P.,

Cortés, J., Pacheco-Riaño, L. C., & Soler, D. (2017).

Lista Roja de Ecosistemas de Colombia. Pontificia

Universidad Javeriana, Conservación Internacional.

https://doi.org/10.13140/RG.2.2.10861.08165

Ewers, R. M., & Didham, R. K. (2006). Confounding fac-

tors in the detection of species responses to habitat

fragmentation. Biological Reviews of the Cambridge

Philosophical Society, 81(1), 117–142. https://doi.

org/10.1017/S1464793105006949

Fahrig, L. (2001). How much habitat is enough? Biological

Conservation, 100(1), 65–74. https://doi.org/10.1016/

S0006-3207(00)00208-1

Fahrig, L. (2003). Effects of habitat fragmentation on bio-

diversity. Annual Review of Ecology, Evolution, and

Systematics, 34(1), 487–515. https://doi.org/10.1146/

annurev.ecolsys.34.011802.132419

522 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

Fahrig, L. (2013). Rethinking patch size and isolation

effects: the habitat amount hypothesis. Journal

of Biogeography, 40(9), 1649–1663. https://doi.

org/10.1111/jbi.12130

Fahrig, L. (2017). Ecological responses to habitat fragmen-

tation per se. Annual Review of Ecology, Evolution,

and Systematics, 48, 1–23. https://doi.org/10.1146/

annurev-ecolsys-110316-022612

Fahrig, L. (2019). Habitat fragmentation: A long and tan-

gled tale. Global Ecology and Biogeography, 28(1),

33–41. https://doi.org/10.1111/geb.12839

Fahrig, L., Arroyo-Rodríguez, V., Bennett, J. R., Boucher-

Lalonde, V., Cazetta, E., Currie, D. J., Eigenbrod, F.,

Ford, A. T., Harrison, S. P., Jaeger, J. A. G., Koper,

N., Martin, A. E., Martin, J. L., Metzger, J. P., Morri-

son, P., Rhodes, J. R., Saunders, D. A., Simberloff,

D., Smith, A. C., … Watling, J. I. (2019). Is habitat

fragmentation bad for biodiversity? Biological Con-

servation, 230, 179–186. https://doi.org/10.1016/j.

biocon.2018.12.026

Fernández, F. (2003). Introdución a las Hormigas de la

región Neotropical. Instituto de Investigación de

Recursos Biológicos Alexander von Humboldt.

Fernández, F., Guerrero, R. J., & Delsinne, T. (2019).

Hormigas de Colombia. Universidad Nacional de

Colombia.

Filgueiras, B. K. C., Melo, D. H. A., Andersen, A. N., Taba-

relli, M., & Leal, I. R. (2019a). Cross-taxon congruen-

ce in insect responses to fragmentation of Brazilian

Atlantic forest. Ecological Indicators, 98, 523–530.

https://doi.org/10.1016/j.ecolind.2018.11.036

Filgueiras, B. K. C., Melo, D. H. A., Leal, I. R., Taba-

relli, M., Freitas, A. V. L., & Iannuzzi, L. (2016).

Fruit-feeding butterflies in edge-dominated habitats:

community structure, species persistence and cas-

cade effect. Journal of Insect Conservation, 20(3),

539–548. https://doi.org/10.1007/s10841-016-9888-4

Filgueiras, B. K. C., Melo, D. H. A., Uehara-Prado,

M., Freitas, A. V. L., Leal, I. R., & Tabarelli, M.

(2019b). Compensatory dynamics on the commu-

nity structure of fruit-feeding butterflies across

hyper-fragmented Atlantic forest habitats. Ecological

Indicators, 98, 276–284. https://doi.org/10.1016/j.

ecolind.2018.11.005

Fischer, J., & Lindenmayer, D. B. (2007). Landscape

modification and habitat fragmentation: a synthesis.

Global Ecology and Biogeography, 16(3), 265–280.

https://doi.org/10.1111/j.1466-8238.2007.00287.x

Forister, M. L., Pelton, E. M., & Black, S. H. (2019).

Declines in insect abundance and diversity: we know

enough to act now. Conservation Science and Practi-

ce, 1, e80. https://doi.org/10.1111/csp2.80

Génier, F. (1998). A revision of the Neotropical genus

Ontherus Erichson (Coleoptera: Scarabaeidae, Scara-

baeinae), Supplement 1. The Coleopterists Bulletin,

52(3), 270–274.

Génier, F., & Kohlmann, B. (2003). Revision of the neo-

tropical dung beetle genera Scatimus Erichson and

Scatrichus gen. noc. (Coleoptera: Scarabaeidae: Sca-

rabaeinae). Fabreries, 28(2), 57–111.

Gilroy, J. J., & Edwards, D. P. (2017). Source-sink dyna-

mics: a neglected problem for landscape-scale

biodiversity conservation in the Tropics. Current

Landscape Ecology Reports, 2(1), 51–60. https://doi.

org/10.1007/s40823-017-0023-3

Giménez-Gómez, V. C., Verdú, J. R., Guerra Alonso, C. B.,

& Zurita, G. A. (2018). Relationship between land

uses and diversity of dung beetles (Coleoptera: Scara-

baeinae) in the southern Atlantic forest of Argentina:

which are the key factors? Biodiversity and Conser-

vation, 27(12), 3201–3213. https://doi.org/10.1007/

s10531-018-1597-8

Gómez-Cifuentes, A., Vespa, N., Semmartín, M., & Zurita,

G. (2020). Canopy cover is a key factor to preser-

ve the ecological functions of dung beetles in the

southern Atlantic Forest. Applied Soil Ecology, 154,

103652. https://doi.org/10.1016/j.apsoil.2020.103652

González, E., Buffa, L., Defagó, M. T., Molina, S. I., Salvo,

A., & Valladares, G. (2018). Something is lost and

something is gained: loss and replacement of species

and functional groups in ant communities at fragmen-

ted forests. Landscape Ecology, 33(12), 2089–2102.

https://doi.org/10.1007/s10980-018-0724-y

González, I., & Déjean, S. (2021). Canonical correlation

analysis (R package version 1.2). https://cran.r-pro-

ject.org/web/packages/CCA/index.html

Hayes, L., Mann, D. J., Monastyrskii, A. L., & Lewis,

O. T. (2009). Rapid assessments of tropical dung

beetle and butterfly assemblages: contrasting trends

along a forest disturbance gradient. Insect Conser-

vation and Diversity, 2(3), 194–203. https://doi.

org/10.1111/j.1752-4598.2009.00058.x

Hernández, J., Guerra Hurtado, A., Ortiz Quijano, R., &

Walschburger, T. (1992). Unidades biogeográficas

de Colombia. In G. Halffter (Ed.), La Diversidad

Biológica de Iberoamérica (pp. 55–105). Instituto de

Ecología, Secretaria de Desarrollo Social, Colombia.

Hernández, O. F., Sánchez, F., & Lizcano, D. J. (2021). Mur-

ciélagos insectívoros aéreos en un paisaje ganadero

del piedemonte llanero colombiano. Biota Colombia-

na, 22(1), 164–183. https://doi.org/10.21068/c2021.

v22n01a11

Horváth, Z., Ptacnik, R., Vad, C. F., & Chase, J. M. (2019).

Habitat loss over six decades accelerates regional

and local biodiversity loss via changing landscape

523

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

connectance. Ecology Letters, 22(6), 1019–1027.

https://doi.org/10.1111/ele.13260

Hsieh, T. C., Ma, K. H., & Chao, A. (2016). iNEXT:

an R package for rarefaction and extrapolation of

species diversity (Hill numbers). Methods in Eco-

logy and Evolution, 7(12), 1451–1456. https://doi.

org/10.1111/2041-210X.12613

IDEAM (Instituto de Investigaciones de Recursos Alexan-

der von Humboldt), SINCHI (Instituto Amazónico

de Investigaciones Científicas), UAESPNN (Unidad

Administrativa Especial del Sistema de Parques

Nacionales Naturales), & IGAC (Instituto Geográ-

fico Agustín Codazzi). (2011). Mapa nacional de

coberturas de la tierra a escala 1:100.000, metodo-

logía Corine Land Cover adaptada para Colombia,

Base de Datos en formato Geodatabase. Convenio

Especial de Cooperación IDEAM, IDEAM, SINCHI,

UAESPNN, IGAC, Colombia.

Jactel, H., Imler, J. L., Lambrechts, L., Failloux, A. B.,

Lebreton, J. D., Maho, Y. Le, Duplessy, J. C., Cossart,

P., & Grandcolas, P. (2021). Insect decline: immediate

action is needed. Comptes Rendus Biologies, 343(3),

267–293. https://doi.org/10.5802/crbiol.37

Jost, L. (2006). Entropy and diversity. Oikos, 113 (2), 363–375.

https://doi.org/10.1111/j.2006.0030-1299.14714.x

Kellner, K. F., Duchamp, J. E., & Swihart, R. K. (2019).

Niche breadth and vertebrate sensitivity to habi-

tat modification: signals from multiple taxa across

replicated landscapes. Biodiversity and Conserva-

tion, 28(10), 2647–2667. https://doi.org/10.1007/

s10531-019-01785-w

Kinzig, A. P., Pacala, S. W., & Tilman, D. (Eds.). (2002).

The functional consequences of biodiversity: empi-

rical progress and theoretical extensions. Princeton

University Press.

Kishimoto-Yamada, K., & Itioka, T. (2015). How much

have we learned about seasonality in tropical insect

abundance since Wolda (1988)? Entomological

Science, 18(4), 407–419. https://doi.org/10.1111/

ens.12134

Lamas, G. (2004). Checklist: Part 4a. Hesperioidea-Papilio-

noidea. In J. B. Heppner (Ed.), Atlas of Neotropical

Lepidoptera (p. 475). Association for Tropical Lepi-

doptera, Inc. Scientific Publishers.

Langevelde, F., Braamburg-Annegarn, M., Huigens, M.

E., Groendijk, R., Poitevin, O., Deijk, J. R., Ellis, W.

N., Grunsven, R. H. A., Vos, R., Vos, R. A., Fran-

zén, M., & WallisDeVries, M. F. (2018). Declines

in moth populations stress the need for conserving

dark nights. Global Change Biology, 24(3), 925–932.

https://doi.org/10.1111/gcb.14008

Latorre, J. P., Rodríguez, O. J., Corredor, L. P., & Arias, D.

A. (2014). Condición de las Unidades Ecobiogeo-

graficas Continentales y Sistema Nacional de Áreas

Protegidas en Colombia (Base de Datos Geográfica

a Escala 1:100.000). Parques Nacionales Naturales

de Colombia.

Laurance, W. F. (2002). Hyperdynamism in fragmen-

ted habitats. Journal of Vegetation Science, 13(4),

595–602. https://doi.org/10.1111/j.1654-1103.2002.

tb02086.x

Losey, J. E., & Vaughan, M. (2006). The econo-

mic value of ecological services provided by

insects. BioScience, 56(4), 311–323. https://doi.

org/10.1641/0006-3568(2006)56[311:TEVOES]2.0.

CO;2

Macdonald, D. W., Chiaverini, L., Bothwell, H. M., Kaszta,

Δ., Ash, E., Bolongon, G., Can, Ö. E., Campos-Arceiz,

A., Channa, P., Clements, G. R., Hearn, A. J., Hedges,

L., Htun, S., Kamler, J. F., Macdonald, E. A., Moore,

J., Naing, H., Onuma, M., Rasphone, A., … Cush-

man, S. A. (2020). Predicting biodiversity richness

in rapidly changing landscapes: climate, low human

pressure or protection as salvation? Biodiversity

and Conservation, 29(14), 4035–4057. https://doi.

org/10.1007/s10531-020-02062-x

MacKenzie, D. I., Nichols, J. D., Royle, J. A., Pollock,

K. H., Bailey, L. L., & Hines, J. E. (2018). Occu-

pancy Estimation and Modeling: Inferring Patterns

and Dynamics of Species Occurrence (2nd Ed.).

Elsevier Academic Press. https://doi.org/10.1016/

C2012-0-01164-7

Mahecha-Jiménez, O., Dumar-Rodríguez, J. C., & Pyrcz,

T. W. (2011). Efecto de la fragmentación del hábitat

sobre las comunidades de Lepidoptera de la tribu

Pronophilini a lo largo de un gradiente altitudinal en

un bosque andino en Bogotá (Colombia) (Lepidop-

tera: Nymphalidae, Satyrinae). SHILAP Revista de

Lepidopterología, 39(153), 117–126.

Mariottini, Y., De Wysiecki, M. L., & Lange, C. E. (2012).

Variación temporal de la riqueza, composición y den-

sidad de acridios (Orthoptera: Acridoidea) en diferen-

tes comunidades vegetales del Sur de la provincia de

Buenos Aires. Revista de la Sociedad Entomológica

Argentina, 71(3–4), 275–288.

Marquez, J. P., & Martínez, N. H. (2020). Estructura

poblacional de Morpho helenor peleides kollar, 1850

(Lepidoptera: Nymphalidae) en un paisaje de bosque

seco tropical, departamento de Bolivar, Colombia.

Boletín Científico. Centro de Museos, 24(2), 169–

189. https://doi.org/10.17151/BCCM.2020.24.2.12

Martínez-Falcón, A. P., Zurita, G. A., Ortega-Martínez, I.

J., & Moreno, C. E. (2018). Populations and assem-

blages living on the edge: Dung beetles responses

to forests-pasture ecotones. PeerJ, 2018(12), e6148.

https://doi.org/10.7717/peerj.6148

Mason, N. W. H., Mouillot, D., Lee, W. G., & Wilson, J. B.

(2005). Functional richness, functional evenness and

functional divergence: the primary components of

524 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

functional diversity. Oikos, 111(1), 112–118. https://

doi.org/10.1111/j.0030-1299.2005.13886.x

Medina, C. A., & Lopera-Toro, A. (2000). Clave ilustrada

para la identificación de géneros de escarabajos

coprófagos (Coleoptera: Scarabaeinae) de Colombia.

Caldasia, 22(2), 299–315. https://doi.org/10.1590/

S1519-566X2009000600002

Melo, D. H. A., Filgueiras, B. K. C., Iserhard, C. A., Ian-

nuzzi, L., Freitas, A. V. L., & Leal, I. R. (2019). Effect

of habitat loss and fragmentation on fruit-feeding

butterflies in the Brazilian Atlantic Forest. Canadian

Journal of Zoology, 97(7), 588–596. https://doi.

org/10.1139/cjz-2018-0202

Minorta-C., V., & Rangel-Ch., J. O. (2015). El clima de la

Orinoquia Colombiana. In J. O. Rangel-Ch. (Ed.),

Colombia Diversidad Biotica XIV. La región de la

Orinoquia de Colombia (pp. 207–236). Universidad

Nacional de Colombia.

Mouillot, D., Mason, W. H. N., Dumay, O., & Wilson, J.

B. (2005). Functional regularity: A neglected aspect

of functional diversity. Oecologia, 142(3), 353–359.

https://doi.org/10.1007/s00442-004-1744-7

Noriega, J. A., Hortal, J., Azcárate, F. M., Berg, M. P.,

Bonada, N., Briones, M. J. I., Del Toro, I., Goulson,

D., Ibanez, S., Landis, D. A., Moretti, M., Potts, S. G.,

Slade, E. M., Stout, J. C., Ulyshen, M. D., Wackers,

F. L., Woodcock, B. A., & Santos, A. M. C. (2018).

Research trends in ecosystem services provided by

insects. Basic and Applied Ecology, 26, 8–23. https://

doi.org/10.1016/j.baae.2017.09.006

Nunes, C. A., Braga, R. F., de Moura Resende, F., de

Siqueira Neves, F., Figueira, J. E. C., & Fernandes, G.

W. (2018). Linking biodiversity, the environment and

ecosystem functioning: ecological functions of dung

beetles along a tropical elevational gradient. Ecosys-

tems, 21(6), 1244–1254. https://doi.org/10.1007/

s10021-017-0216-y

Nunes, C. A., Braga, R. F., Figueira, J. E. C., Neves, F. de

S., & Fernandes, G. W. (2016). Dung beetles along a

tropical altitudinal gradient: environmental filtering

on taxonomic and functional diversity. PLoS ONE,

11(6), e0157442. https://doi.org/10.1371/journal.

pone.0157442

Oksanen, J., Guillaume Blanchet, F., Kindt, R., Legendre,

P., Minchin, P. R., O’Hara, R. B., Simpson, G. L.,

Solymos, P., Stevens, M. H., & Wagner, H. (2019).

Vegan: Community Ecology Package (R package ver-

sion 2.5-6). https://cran.r-project.org/package=vegan

Parikh, G., Rawtani, D., & Khatri, N. (2020). Insects as an

indicator for environmental pollution. Environmental

Claims Journal, 33(2), 161–181. https://doi.org/10.1

080/10406026.2020.1780698

Pla, L., Casanoves, F., & Di Rienzo, J. A. (2012). Quanti-

fying Functional Biodiversity. Springer. https://doi.

org/10.1007/978-94-007-2648-2

Püttker, T., Bueno, A. A., dos Santos de Barros, C., Som-

mer, S., & Pardini, R. (2011). Immigration rates in

fragmented landscapes - empirical evidence for the

importance of habitat amount for species persistence.

PLoS ONE, 6(11), e27963. https://doi.org/10.1371/

journal.pone.0027963

Püttker, T., Crouzeilles, R., Almeida-Gomes, M., Schmoe-

ller, M., Maurenza, D., Alves-Pinto, H., Pardini, R.,

Vieira, M. V., Banks-Leite, C., Fonseca, C. R., Metz-

ger, J. P., Accacio, G. M., Alexandrino, E. R., Barros,

C. S., Bogoni, J. A., Boscolo, D., Brancalion, P. H.

S., Bueno, A. A., Cambui, E. C. B., … Prevedello, J.

A. (2020). Indirect effects of habitat loss via habitat

fragmentation: A cross-taxa analysis of forest-depen-

dent species. Biological Conservation, 241, 108368.

https://doi.org/10.1016/j.biocon.2019.108368

Queiroz, A. C. M., Rabello, A. M., Braga, D. L., Santiago,

G. S., Zurlo, L. F., Philpott, S. M., & Ribas, C. R.

(2020). Cerrado vegetation types determine how land

use impacts ant biodiversity. Biodiversity and Con-

servation, 29(1), 2017–2034. https://doi.org/10.1007/

s10531-017-1379-8

Queiroz, A. C. M., & Ribas, C. R. (2016). Canopy

cover negatively affects arboreal ant species rich-

ness in a tropical open habitat. Brazilian Jour-

nal of Biology, 76(04), 864–870. https://doi.

org/10.1590/1519-6984.02015

R Core Team. (2019). R: A Language and Environment for

Statistical Computing. R Foundation for Statistical

Computing. https://www.r-project.org

Rangel-Ch., J. O. (2014). Ecosistemas de la Orinoquia

Colombia. In J. O. Rangel-Ch. (Ed.), Colombia.

Diversidad Biótica XIV. La región de la Orinoquia

de Colombia (pp. 807–847). Universidad Nacional

de Colombia.

Rangel-Ch., J. O., & Minorta-C., V. (2015). Los tipos de

vegetación de la Orinoquia Colombiana. In J. O. Ran-

gel-Ch. (Ed.), Colombia Diversidad Biotica XIV. La

región de la Orinoquia de Colombia (pp. 533–608).

Universidad Nacional de Colombia.

Rivera, L. F., Botero, M., Escobar, S., & Armbrecht, I.

(2008). Diversidad de hormigas en sistemas gana-

deros. In E. Murgueitio, C. Cuartas, & J. Naranjo

(Eds.), Ganadería del futuro : investigación para el

desarrollo (pp. 227–243). Fundación CIPAV.

Romero, M. H., Galindo, G., Otero, J., & Armenteras,

D. (2004). Ecosistemas de la cuenca del Orinoco

colombiano. Instituto de Investigación de Recursos

Biológicos Alexander von Humboldt.

Sackmann, P. (2006). Efectos de la variación temporal y los

métodos de captura en la eficiencia de un muestreo de

525

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 504-525, Enero-diciembre 2022 (Publicado Ago. 09, 2022)

coleópteros en la Reserva Natural Loma del Medio,

El Bolsón, Río Negro. Revista de la Sociedad Ento-

mológica Argentina, 65(3–4), 35–50.

Sanabria-Blandón, M. C., & de Ulloa, P. (2011). Hormigas

cazadoras en sistemas productivos del piedemonte

amazónico colombiano: diversidad y especies indica-

doras. Acta Amazonica, 41(4), 503–512.

Sánchez-Bayo, F., & Wyckhuys, K. A. G. (2019). World-

wide decline of the entomofauna: A review of its

drivers. Biological Conservation, 232, 8–27. https://

doi.org/10.1016/j.biocon.2019.01.020

Santoandré, S., Filloy, J., Zurita, G. A., & Bellocq, M. I.

(2019). Taxonomic and functional β-diversity of ants

along tree plantation chronosequences differ between

contrasting biomes. Basic and Applied Ecology, 41,

1–12. https://doi.org/10.1016/j.baae.2019.08.004

Sardanyés, J., Piñero, J., & Solé, R. (2019). Habitat loss-

induced tipping points in metapopulations with faci-

litation. Population Ecology, 61(4), 436–449. https://

doi.org/10.1002/1438-390X.12020

Sarmiento-Garcés, R. & Amat-García, G. (2014). Esca-

rabajos del género Dichotomius Hope 1838 (Scara-

baeidae: Scarabaeinae) en Colombia. Universidad

Nacional de Colombia.

Scholtz, C. H., Davis, A. L. V., & Kryger, U. (2009). Evolu-

tionary biology and conservation of dung beetles (1st

Ed.). Pensoft Publishers.

Senior, R. A., Hill, J. K., González del Pliego, P., Goode, L.

K., & Edwards, D. P. (2017). A pantropical analysis

of the impacts of forest degradation and conversion

on local temperature. Ecology and Evolution, 7(19),

7897–7908. https://doi.org/10.1002/ece3.3262

Skogen, K., Helland, H., & Kaltenborn, B. (2018). Con-

cern about climate change, biodiversity loss, habitat

degradation and landscape change: Embedded in

different packages of environmental concern? Jour-

nal for Nature Conservation, 44, 12–20. https://doi.

org/10.1016/j.jnc.2018.06.001

Spector, S. (2006). Scarabaeine dung beetles (coleoptera:

Scarabaeidae: Scarabaeinae): an invertebrate focal

taxon for biodiversity research and conservation.

The Coleopterists Bulletin, 60(5), 71–83. https://doi.

org/10.1649/0010-065x(2006)60[71:sdbcss]2.0.co;2

Stork, N. E. (2018). How many species of insects and other

terrestrial arthropods are there on Earth? Annual

Review of Entomology, 63(1), 31–45. https://doi.

org/10.1146/annurev-ento-020117-043348

Suárez-Parra, K. V., Cély-Reyes, G. E., & Forero-Ulloa, F.

E. (2016). Corine Land Cover (CLC) methodology

validation for the space temporary coverage deter-

mination: Mecha creek case (Cómbita, Boyacá),

Colombia. Biota Colombiana, 17(1), 1–15. https://

doi.org/10.21068/C2016v17r01a01

USGS (United States Geological Survey). (2019). Imagen

Satelital 7-57 de Landsat. https://glovis.usgs.gov/app

Vargas-Zapata, M. A., Martínez-Hernández, N. J., Gutié-

rrez-Moreno, L. C., Prince-Chacon, S., Herrera-

Colon, V., & Torres-Periñan, L. F. (2011). Species

richness and abundance of Hesperioidea and Papi-

lionoidea (Lepidoptera) in Las Delicias Natural

Reserve, Santa Marta, Magdalena, Colombia. Acta

Biológica Colombiana, 16(1), 43–60. https://doi.

org/10.15446/abc

Vaz de Mello, F. Z., Edmonds, W. D., Ocampo, F. C., &

Schoolmeesters, P. (2011). A multilingual key to the

genera and subgenera of the subfamily Scarabaeinae

of the New World (Coleoptera: Scarabaeidae). Zoo-

taxa, 2854(2854), 1–73. https://doi.org/10.11646/

zootaxa.2854.1.1

Velosa, R. I., Domínguez, K. J., & Romero, Y. (2018).

Composición y diversidad del banco de semillas en

áreas urbanas fragmentadas de piedemonte, Villavi-

cencio, Colombia. Ingenierías USBMed, 9(1), 86–96.

https://doi.org/10.21500/20275846.3317

Villarreal, H., Álvarez, M., Córdoba, S., Escobar, F., Fagua,

G., Gast, F., Mendoza, H., Ospina, M., & Umaña, A.

M. (2006). Manual de métodos para el desarrollo

de inventarios de biodiversidad (2nd Ed.). Instituto

de Investigación de Recursos Biológicos Alexander

von Humboldt.

Wagner, D. L. (2020). Insect declines in the anthropocene.

Annual Review of Entomology, 65, 457–480. https://

doi.org/10.1146/annurev-ento-011019-025151

Warren, A. D., Davis, K. J., Stangeland, E. M., Pelham, P. J.,

Willmott, K. R., & Grishin, N. V. (2017). Illustrated

Lists of American Butterflies (North and South Ame-

rica). Butterflies of America Foundation.

Watling, J. I., Arroyo-Rodríguez, V., Pfeifer, M., Baeten,

L., Banks-Leite, C., Cisneros, L. M., Fang, R.,

Hamel-Leigue, A. C., Lachat, T., Leal, I. R., Lens,

L., Possingham, H. P., Raheem, D. C., Ribeiro, D. B.,

Slade, E. M., Urbina-Cardona, J. N., Wood, E. M.,

& Fahrig, L. (2020). Support for the habitat amount

hypothesis from a global synthesis of species density

studies. Ecology Letters, 23(4), 674–x681. https://doi.

org/10.1111/ele.13471