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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(4): 1289-1305, October-December 2021 (Published Dec. 17, 2021)

Vertical stratification of arthropods in the dry ecosystems of Colombian

Guyana: morphological patterns and their ecological implications

Edgar Camero Rubio1*; https://orcid.org/0000-0002-4639-0564

Johanna Paola Cárdenas2; https://orcid.org/0000-0002-9379-7818

Jaime Marín Ballesteros1; https://orcid.org/0000-0001-9062-1852

1. Departamento de Biología, Universidad Nacional de Colombia, Bogotá D. C., Colombia; eecameror@unal.edu.co

(*Correspondence), jmarinb@unal.edu.co

2. Departamento de Biología, Universidad Pedagógica Nacional, Bogotá D. C., Colombia; jpcardenash@unal.edu.co

Received 08-VIII-2021. Corrected 18-XI-2021. Accepted 10-XII-2021.

ABSTRACT

Introduction: Despite growing interest by the ecosystems derived from the Guyanese formations, the vertical

structure of the communities and relationships of the biota with the climatic conditions in these ecosystems are

unknown.

Objective: Characterize the structure and vertical composition of the arthropod fauna associated with three of

the most representative ecosystems of the Northern area of the serranía de La Lindosa in Colombia based on

morphological and ecological parameters.

Methods: The arthropod fauna was sampled, from the subsurface soil level to the shrub and tree stratum. The

fauna was determined up to the level of family or supraspecific group and the values of Alfa and Beta diversity

were determined. Body length measurements were made, and the coloration and trophic level of each group

were determined.

Results: The composition and diversity of the arthropod fauna was different in each ecosystem and vertical

stratum and most of the groups in all the ecosystems studied present low abundances. Groups of phytophagous

and predatory habits were frequent in all ecosystems and the highest biomass of arthropod fauna comes from

groups of polyphagous habits, of medium size and great abundance. Light and dark colorations are the most

frequent in landscape-scale.

Conclusion: The ecosystems studied are characterized by the low values of diversity and replacement and

the large number of non-shared groups that apparently respond to the microclimatic characteristics; however,

there are some generalities on a landsc ape scale such as the greater richness and abundance of groups in the

intermediate strata, the greater proportion of groups with phytophagous habits and medium body sizes, and the

predominance of dark colorations in the lower strata.

Key words: arthropods; vertical stratification; functional groups; trophic guilds; Colombian Guyana.

Camero Rubio, E., Cárdenas, J. P., & Marín Ballesteros, J.

(2021). Vertical stratification of arthropods in the dry

ecosystems of Colombian Guyana: morphological patterns

and their ecological implications. Revista de Biología

Tropical, 69(4), 1289-1305. https://doi.org/10.15517/rbt.

v69i4.48024

https://doi.org/10.15517/rbt.v69i4.48024

ECOLOGÍA TERRESTRE

Arthropods are the most diverse group of

animals in nature. Their evolutionary history

has allowed them to adapt to all the climates

and ecosystems on the planet where they per-

form different functions by virtue of the multi-

plicity of their habits. Although they have been

studied in almost all their aspects, their ecol-

ogy, the preference of their habitats and their

adaptations to environmental demands are the

source of recent studies (Chown & Nicolson,

2004; Dillon & Lozier, 2019). Factors such as

temperature, the amount of light, exposure to

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rain and wind, as well as the quantity and qual-

ity of available resources, influence their distri-

bution in the different stratum of tropical forests

(Basset et al., 2003). The influence of climate

on insects for example, triggers a series of mor-

pho-physiological transformations that include

strategies of evasion, adaptation, or resistance

with great ecological and evolutionary impli-

cations (Colinet et al., 2015; Danks, 2007).

Characteristics such as size and color patterns

in insects can influence inter- and intraspecific

competition, thermoregulation, activity levels,

and resource use (Gentile et al., 2021; Peters,

1983), since ectothermic organisms depend

on external sources of heat for the internal

regulation of their body temperature (Chown &

Nicolson, 2004; Forsman et al., 2008).

The Colombian Guyana is part of the

Western biogeographic province of the Guiana

Shield that is subdivided into five districts and

12 endemic areas (Hernández et al., 1992). Its

geoforms are made up of rocky outcrops with

very shallow soils with little vegetation cover,

steep slopes, and the evident influence of physi-

cal weathering, made up of a series of mountain

ranges, mountains, hills, and savannas, among

which those of Chiribiquete, La Macarena, El

Tuparro, Araracuara, Taraira, Naquén, Lajas de

Guainía and La Lindosa stand out, which were

linked in the Tertiary to the Guiana and Bra-

zilian shields (Gentry, 1982; Giraldo-Cañas,

2001) so they share much of their floristic and

fauna, in addition to a many endemisms (Cam-

ero, 2019; Giraldo-Cañas, 2001).

The Sierra de La Lindosa is a low moun-

tain range located in the transitional zone

between the large regions of Orinoquia and the

Colombian Amazon and greatly affects region-

al climatic characteristics. The soils are derived

from sedimentary rocks of Cretaceous age that

contain a high content of iron that gives them

a reddish color. They are loamy to sandy soils,

little-evolved and well-drained, with an acidic

pH, not very fertile, and with low nutrient

content (Botero et al., 2018). The climatic and

soil characteristics favor the development of

low forests, open bushes and savannas with

varied herbaceous elements, such as shrubs and

stunted trees that tend to be perennial, leathery,

and with a marked xeromorphic appearance

(Hernández & Sánchez, 1992). The typical

vegetation of the low forests is composed of

communities of a few individual trees with

irregular canopies and very little cover, with

heights of up to 8 m. The bushes are located

on the rocky outcrops and are composed of few

species in general belonging to the families:

Annonaceae, Asteraceae, Bonnetiaceae, Clusi-

aceae, Melastomataceae, Myrtaceae, Rubiace-

ae, and Tepuianthaceae and herbaceous species

of the genera: Aechmea, Anemia, Axonopus,

Diacidia, Navia, Selaginella, Schizachyrium

and Vellozia. The savannas are made up of

different types of communities, among which:

Aeschynomene, Andropogon, Axonopus, Bul-

bostylis, Calea, Clitoria, Desmodium, Drosera,

Hyptis, Nautilocalyx, Otachyrium, Panicum,

Paspalum, Sipanea, Sipaneopsis, Siphantera,

Trachypogon, Utricularia and Xyris species

stand out (Giraldo-Cañas, 2001).

Despite the great interest aroused by

the particularities of the ecosystems that are

formed under the climatic conditions of the

Guiana Shield, most of the research that has

been accomplished in this region covers vege-

tational aspects and analyze the composition of

insect and invertebrate faunas and other animal

groups. But there is little research that seeks

to establish adaptations of biota to this type of

environment that has great climatic demands.

The present research seeks to establish the dif-

ferences in the conformation of the arthropod

fauna found under the most representative plant

communities in the Northern parts of the Sierra

de La Lindosa mountain range in Colombia,

based on the variations in the ecological param-

eters and on some morphological attributes,

under the hypothesis of the evident climatic

incidence in the structure and adaptations of

arthropod communities.

MATERIALS AND METHODS

Study area: The Sierra de La Lindosa

has an area of 12 000 hectares and is located

within the Guaviare geographical region in

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Colombia; it is geologically influenced by the

Guiana Shield and climatically influenced by

the Orinoquia and Amazonian regions. The

regional climate has a mean temperature of

25.7 °C with a variation of less than 2 °C and a

mean annual range of precipitation of between

3 000 to 4 000 mm with a monomodal climatic

regime, with the greatest precipitation between

the months of May and June and the lowest

rainfall between the months of January and

February (IGAC, 1979). Under these condi-

tions, different pedobiomes develop that range

from lithophytic forests and xerophytic scrub

to different types of savannas that are matrices

of a great variety of ecological landscapes

(Hernández & Sánchez, 1992). The mountain

range is located near the municipality of San

José del Guaviare where three sampling sta-

tions belonging to three different plant com-

munities were located: casmophytic savannas

(M1) located at 2°30’45” N & 72°42’52” W

at 320 m.a.s.l.; xerophytic scrub (M2) located

between 2°30’42” N & 72°42’41” W at 345

m.a.s.l. and lithophytic forests (M3) located

between 2°30’12” N & 72°41’17” W at 315

m.a.s.l. (Fig. 1).

Sampling and data analysis: Arthropods

captures were made in four vertical strata dur-

ing years 2014 and 2015: 1) subsurface soil

without vegetation from 0 to 20 cm deep, 2)

herbaceous or litter layer, 3) shrub stratum, and

4) canopy above 10 m. For the subsurface stra-

tum, five samples were analyzed by the extrac-

tion of 1 kg of soil per sample using Berlese

funnels (Berlese, 1905; Tullgren, 1918). For

the capture of organisms from the herbaceous

stratum ten pitfall traps of 500 ml were located

in a straight line and separated by distances

of 10 m within random transects (Greenslade,

1964; Sabu et al., 2011). The samplings in

the shrub stratum were carried out using two

intensive methods: 1) 6 replications of 100

entomological net passes on the vegetation,

and 2) the installation of flight interception

traps with volatile bait at a height of 2 m (Peck

& Davies, 1980). A variation of the latter trap

was used above 10 m to capture arthropods in

the canopy stratum for a minimum time of 48

hours. Physicochemical analyses were carried

out for soil samples, including the texture, pH,

conductivity, amount of organic matter (OM),

percentage of roots, humidity, porosity, and

field capacity (CC) and these were related to

the fauna collected in the edaphic strata. For

the other stratum the variables temperature and

relative humidity were measured by means of a

conventional multimeter.

Samples by stratum and ecosystem were

labeled and transported in 70 % alcohol to the

Fig. 1. Location of the sampling stations in the La Lindosa mountains - Colombia.

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Ecology Laboratory of the National University

of Colombia for the measurement of the mor-

pho-ecological characteristics and for the taxo-

nomic determination to family or supraspecific

group by using the keys from Grimaldi and

Engel (2005), Gullan and Craston (2010) and

Johnson and Triplehorn (2005), and confirming

the valid names in Species 2000 and in the ITIS

Catalog (Roskov et al., 2019).

For the ecomorphological attributes, tro-

phic guilds were assigned for each group after

bibliographic consultations. The average body

length of each of the collected groups was

evaluated since head to apice abdomen, as well

as the coloration according to the following

numerical range: 1- for white-yellow-cream

colors, 2- for black-brown, 3- for orange-

red and 4- for blue-green. Biomass (Bc) was

evaluated using a formula proposed by Stork

and Blackburn (1993), that considers the num-

ber of individuals (N) and the average body

length (L):

Bc = N (0.0305 L2.62)

The trophic levels of the fauna were

included in eight categories according to Price

(1984): phytophagous, polyphage, fungivores,

dung, saprophagus, hematophage, predator and

parasites/parasitoids, including within the phy-

tophagous habits those groups of arthropods,

especially insects, that feed on various plant

organs and that contemplate defoliators, chop-

pers, suckers, and miners.

For data analysis we evaluated the effi-

ciency of the sampling by means of the Chao-1

estimator to find the richness completeness of

groups by relating the observed species rich-

ness with the estimated richness and by the

negative binomial method using the richness

values of the groups in the different sample

units. Additionally, we carried out an explor-

atory box-plot analysis to evaluate the similari-

ties between ecosystems (Chao & Jost, 2012;

Magurran, 1989). Abundance models from the

richness values of the collected groups were

determined, as well as Bray-Curtis similarity

dendrograms from the abundance data through

the single-linkage method, and the Brillouin

diversity values (B) most recommended for

this type of sampling (Magurran, 1989). The

Simpson dominance (D) and fairness (1-D) and

Wittaker beta diversity values (aW) between

ecosystems and layers were calculated from

abundance values of the groups by using the

STATS (Bolar, 2019), MASS (Ripley et al.,

2020) and CAR (Fox et al., 2020) packages in

the R programming language v. 4.0.3 (R Devel-

opment Core Team, 2017), validated using

Kruskal-Wallis tests. A canonical correspon-

dence analysis (CCA) was made to determine

the relationship between the physicochemical

factors and the collected groups. Finally, we

established the total distribution of biomass in

relation to the associations in each ecosystem

and determined the affinity of the fauna to the

sampling sites by means of a correspondence

analysis (DCA) using the PAST software v.

2.15 (Hammer et al., 2001).

RESULTS

Abundance and diversity: We collected

4 276 individuals in the study area including

18 orders and 112 families or supraspecific

groups (Table 1). We collected 48 % of the

individuals in the xerophytic scrub, 27 % in the

casmophytic savanna, and the remaining 25 %

in the lithophytic forest. Of the 112 groups col-

lected, 83 were obtained in the savanna, 68 in

the scrub and 63 in the forest. Although there

are differences in the diversity values between

the three sampling points (Kruskal-Wallis, H

= 7.3, P = 0.05) and between ecosystem lay-

ers, diversity at the landscape level is low and

with low replacement values (aW); however,

these results may vary throughout the climatic

seasons. The highest faunal diversity and group

equitability was obtained in the casmophyte

savanna (M1) (HB = 3.15; 1-D = 0.89) and the

lowest diversity was from the scrub (M2) (HB

= 2.48) that at the same time had the highest

dominance values (D = 0.25) (Table 2).

The abundance and composition of the

groups varied from one ecosystem to another

and between each of the vertical stratum. At

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TABLE 1

Trophic guilds, colorations and relative abundances for arthropod fauna from ecosystems studied in the La Lindosa

mountains

Family/Group T. guild Color Cas_

savanna

Xeroph_

Scrub

Lith_

Forest Family/Group T. guild Color Cas_

savanna

Xeroph_

Scrub

Lith_

Forest

1 Acari Pol 2 0.0104 0.0049 0.0047 92 Lonchopteridae Phyt 1 0.0060 - -

2 Acari Pol 1 0.0009 0.0019 0.0056 93 Lygaeidae Phyt 2 0.0026 - -

3 Acrididae Phyt 2 0.0035 0.0005 0.0019 94 Mantidae Pred 1 0.0009 - -

4Aeolothripidae Phyt 2 - - 0.0028 95 Mantidae Pred 2 0.0009 0.0005 -

5 Agromyzidae Phyt 2 - - 0.0019 96 Mantidae Pred 4 0.0017 - -

6 Agromyzidae Phyt 2 - 0.0039 - 97 Membracidae Phyt 2 0.0009 - -

7 Anthophoridae Sap 2 - 0.0010 - 98 Membracidae Phyt 1 0.0009 - -

8 Aphididae Phyt 1 0.0078 - 0.0009 99 Membracidae Phyt 3 0.0294 - -

9 Apidae Phyt 2 0.0112 - - 100 Miridae Phyt 2 0.0112 0.0005 -

10 Apidae Phyt 1 0.0095 0.0233 - 101 Muscidae Dung 2 0.0017 0.0034 0.0094

11 Aranae Pred 1 0.0233 0.0161 0.0198 102 Mycetophilidae Fung 1 0.0026 0.0010 -

12 Aranae Pred 2 0.0009 0.0019 0.0038 103 Mycetophilidae Fung 2 0.0017 0.0024 0.0009

13 Argidae Phyt 1 - - 0.0019 104 Mymaridae Psd 2 - - 0.0009

14 Asilidae Pred 2 - 0.0005 - 105 Mymaridae Psd 1 - 0.0010 -

15 Blattidae Phyt 1 0.0017 - 0.0028 106 Nitidulidae Phyt 1 - 0.0078 0.2825

16 Blattidae Pol 2 - 0.0005 0.0056 107 Nitidulidae Phyt 2 0.0181 - 0

17 Blattidae Pol 1 - 0.0005 - 108 Oligotomidae Phyt 2 0.0009 - 0.0009

18 Braconidae Psd 1 - 0.0024 0.0028 109 Onychiuridae Sap 1 0.0009 0.0010 0.0019

19 Buprestidae Pol 1 0.0017 - - 110 Otididae Phyt 2 0.0026 - 0.0019

20 Carabidae Pred 2 - 0.0005 - 111 Pentatomidae Phyt 1 0.0017 - -

21 Cecidomyiidae Phyt 2 0.0043 - 0.0019 112 Pentatomidae Phyt 2 0.0035 - -

22 Cecidomyiidae Phyt 1 0.0052 0.0058 0.0358 113 Pergidae Hem 2 0.0009 - -

23 Ceratopogonidae Hem 2 0.0535 0.0034 0.0235 114 Phoridae Sap 1 0.0017 0.0058 0.0217

24 Ceratopogonidae Hem 1 0.0086 0.0005 0.0019 115 Phoridae Sap 2 0.0026 0.0165 0.0056

25 Cercopidae Phyt 1 0.0173 - - 116 Piesmatidae Phyt 2 - 0.0005 -

26 Chalcidoidea Psd 2 0.0121 0.0019 0.0104 117 Pompilidae Pred 2 - 0.0005 -

27 Chalcidoidea Psd 1 0.0086 0.0024 - 118 Proscopiidae Phyt 1 0.0009 - -

28 Chironomidae Phyt 1 0.0026 0.0010 0.0019 119 Proscopiidae Phyt 2 - - 0.0009

29 Chironomidae Phyt 2 0.0009 0.0005 0.0038 120 Proscopiidae Phyt 2 0.0026 - -

30 Chrysomelidae Phyt 1 0.0026 0.0010 0.0009 121 Pselaphidae Pred 1 0.0017 0.0005 -

31 Chrysomelidae Phyt 2 0.0009 0.0010 0.0047 122 Psocoptera Pol 1 - 0.0010 -

32 Chrysomelidae Phyt 4 - 0.0010 0.0009 123 Psychodidae Pol 1 0.0026 - 0.0009

33 Chrysopidae Phyt 4 0.0009 - - 124 Psychodidae Hem 1 0.0017 - 0.0009

34 Chrysopidae Phyt 1 0.0060 - - 125 Ptiliidae Fung 2 0.0017 0.0068 -

35 Cicadellidae Phyt 1 0.0060 - 0.0009 126 Ptiliidae Fung 1 0.0130 - -

36 Cicadellidae Phyt 2 0.0017 0.0015 - 127 Reduviidae Hem 3 0.0035 - 0.0009

37 Cicadellidae Phyt 3 - - 0.0019 128 Reduviidae Hem 1 0.0009 - 0.0009

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Family/Group T. guild Color Cas_

savanna

Xeroph_

Scrub

Lith_

Forest Family/Group T. guild Color Cas_

savanna

Xeroph_

Scrub

Lith_

Forest

38 Crabronidae Phyt 1 0.0009 - - 129 Reduviidae Hem 4 0.0043 - -

39 Culicidae Hem 1 0.0181 0.0049 0.0395 130 Reduviidae Hem 2 - 0.0005 0.0019

40 Culicidae Hem 2 0.0035 0.0058 0.0028 131 Rhagionidae Pred 2 0.0035 0.0005 -

41 Culicidae Hem 1 - 0.0039 - 132 Richardiidae Phyt 1 - 0.0005 -

42 Curculionidae Phyt 2 0.0155 0.0019 0.0047 133 Riodinidae Phyt 4 0.0250 0.0092 0.0160

43 Curculionidae Phyt 1 0.0086 - 0.0141 134 Scarabaeidae Dung 1 - - 0.0009

44 Cydnidae Phyt 2 0.0026 0.0224 0.0009 135 Scarabaeidae Dung 4 - - 0.0019

45 Cydnidae Phyt 1 - - 0.0009 136 Scarabaeidae Dung 2 0.0017 - 0.0038

46 Cynipidae Phyt 2 - - 0.0009 137 Scarabaeidae Dung 1 - 0.0010 -

47 Delphacidae Phyt 1 0.0276 - - 138 Scarabaeidae Dung 2 - 0.0019 -

48 Dictyopharidae Phyt 1 0.0009 - 0.0009 139 Sciaridae Fung 1 0.0112 0.0015 0.0019

49 Dipsocoridae Pred 1 0.0017 - - 140 Sciaridae Fung 2 0.0095 0.0034 0.0047

50 Dipsocoridae Pred 2 - - 0.0009 141 Sciomyzidae Phyt 1 - - 0.0009

51 Dixidae Phyt 1 0.0302 - - 142 Scolytidae Xyl 2 0.0052 0.0005 0.0009

52 Dolichopodidae Pred 2 0.0009 0.0068 0.0028 143 Scolytidae Xyl 2 - 0.0131 -

53 Dolichopodidae Pred 4 0.0009 - 0.0019 144 Scolytidae Xyl 1 - 0.0044 -

54 Drosophilidae Phyt 2 0.0009 0.0112 0.0104 145 Scorpiones Pred 2 0.0009 - -

55 Drosophilidae Phyt 1 0.0017 0.0024 0.0019 146 Scydmaenidae Pred 1 0.0009 0.0015 -

56 Drosophilidae Phyt 3 - - 0.0056 147 Simuliidae Phyt 1 - 0.0015 0.0009

57 Elateridae Phyt 1 - 0.0010 0.0009 148 Simuliidae Phyt 2 - 0.0005 -

58 Elateridae Phyt 2 - - 0.0009 149 Sminthuridae Sap 3 0.0017 0.0010 -

59 Embiidina Phyt 1 - - 0.0009 150 Sminthuridae Sap 2 - 0.0088 0.0085

60 Empididae Phyt 2 - - 0.0047 151 Sminthuridae Sap 1 0.0026 0.0088 0.0734

61 Entomobryidae Sap 1 0.0121 0.0063 0.0330 152 Sminthuridae Sap 4 - 0.0029 -

62 Entomobryidae Sap 2 - 0.0010 - 153 Sphaeroceridae Sap 2 0.0043 - 0.0019

63 Ephydridae Phyt 1 - - 0.0009 154 Sphaeroceridae Sap 1 0.0009 - -

64 Ephydridae Phyt 2 0.0069 0.0005 0.0028 155 Sphaeroceridae Sap 2 - 0.0005 -

65 Eulophidae Psd 2 0.0026 - - 156 Sphecidae Sap 2 0.0009 - -

66 Eurytomidae Psd 2 - 0.0005 - 157 Staphylinidae Pol 2 0.0026 0.0083 0.1318

67 Flatidae Phyt 2 - - 0.0009 158 Staphylinidae Pol 1 0.0190 0.0136 0.0198

68 Forficulidae Phyt 2 0.0017 - - 159 Stratiomyidae Sap 2 - 0.0005 -

69 Formicidae Phyt 1 0.0043 0.0438 0.0113 160 Syrphidae Phyt 2 0.0104 0.0019 -

70 Formicidae Pol 2 0.3066 0.6308 0.0678 161 Tabanidae Hem 2 - 0.0005 -

71 Formicidae Phyt 3 - - 0.0019 162 Tachinidae Psd 2 0.0242 0.0010 0.0009

72 Fulgoroidea Phyt 1 0.0173 0.0019 0.0151 163 Tenthredinidae Phyt 1 0.0009 - -

73 Fulgoroidea Phyt 2 0.0009 0.0005 0.0009 164 Tephritidae Dung 2 0.0009 - 0.0038

74 Fulgoroidea Phyt 3 - - 0.0009 165 Termitidae Xyl 1 - - 0.0019

75 Geometridae Phyt 2 0.0017 - - 166 Tetrigidae Phyt 1 0.0043 - -

76 Gryllacrididae Pred 1 - - 0.0009 167 Tettigoniidae Phyt 1 0.0009 - -

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Family/Group T. guild Color Cas_

savanna

Xeroph_

Scrub

Lith_

Forest Family/Group T. guild Color Cas_

savanna

Xeroph_

Scrub

Lith_

Forest

77 Gryllacrididae Phyt 4 0.0043 - - 168 Tettigoniidae Phyt 2 - 0.0010 -

78 Gryllidae Pol 2 0.0535 - - 169 Therevidae Hem 2 0.0009 - -

79 Gryllidae Pol 1 - - 0.0009 170 Thripidae Phyt 1 0.0009 0.0044 0.0009

80 Gryllotalpidae Pred 1 0.0017 - 0.0019 171 Thripidae Phyt 2 - 0.0005 -

81 Gryllotalpidae Phyt 4 - - 0.0019 172 Tingidae Phyt 2 - 0.0005 -

82 Halictidae Phyt 4 0.0017 - - 173 Tipulidae Phyt 1 - 0.0019 0.0009

83 Histeridae Pred 2 - 0.0005 - 174 Tipulidae Phyt 2 - - 0.0028

84 Hydrophilidae Phyt 2 - 0.0117 0.0038 175 Torymidae Phyt 2 - - 0.0009

85 Isopteridae Sap 1 - 0.0131 - 176 Trichogrammatidae Psd 2 0.0009 - -

86 Isopteridae Sap 5 - 0.0015 - 177 Trogidae Pol 2 - 0.0005 -

87 Labiduridae Sap 2 0.0009 0.0015 - 178 Ulidiidae Phyt 2 - - 0.0019

88 Labiidae Sap 1 0.0009 - - 179 Veliidae Phyt 2 0.0026 - -

89 Laemophloeidae Phyt 1 - - 0.0009 180 Vespidae Pred 1 0.0009 - -

90 Lauxaniidae Phyt 1 0.0009 0.0005 - 181 Vespidae Pred 2 - - 0.0009

91 Lauxaniidae Phyt 2 0.0026 0.0019 - 182 Vespidae Pred 1 - 0.0005 -

Exclusive groups are highlighted in bold. Trophic guilds: Phyt: phytophagous, Pol: polyphage, Fung: fungivores, Dung,

Sap: saprophagus, Xyl: xylophagous, Hem: hematophagous, Pred: predator, Psd: parasites/parasitoids. Body colorations: 1:

white-yellow-cream, 2: black-brown, 3: orange-red, 4: blue-green.

TABLE 2

Diversity estimators for the ecosystems studied in the La Lindosa mountains - Colombia

Alpha diversity

Casm_Savanna (M1) Xeroph_Scrub (M2) Lith_Forest (M3)

Taxa 113 95 96

Individuals (n) 1158 2056 1062

Dominance (D) 0.12 0.25 0.12

Simpson (1-D) 0.89 0.74 0.88

Brillouin (HB) 3.15 2.48 2.85

Chao-1 140 120.4 126.3

Compl (%) 80.7 78.9 76.0

Beta diversity (aW)

Casm_Savanna Xeroph_Scrub Lith_Forest

Casm_Savanna 0 0.47115 0.45455

Xeroph_Scrub 0.47115 0 0.47644

Lith_Forest 0.45455 0.47644 0

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the ecosystem level (and in general for its

stratum) there was an equitable distribution of

abundance between the dominant groups and

the few exclusive low-abundance groups that

can be seen in the graphs of the abundance

models and in their greater adjustment to the

logarithmic models. The expected richness in

the sampling sites was higher than that found

according to the values in the Chao-1 index,

from which the calculation of the percentage

of completeness is derived and that was higher

in the savanna ecosystem (80.7 %) and lower

in the forest ecosystem (76.0 %); so, most of

the richness of the arthropod fauna in the study

area was collected through the sampling tech-

niques used. Relative abundances of arthropod

fauna for each ecosystem are observed in

Table 1. In the case of exclusive groups, these

represent between 15 and 30 % of the fauna

collected in the three ecosystems, suggesting a

very similar fauna composition in all of them

(Fig. 2A, Fig. 2B), reflected in the mean values

of beta diversity and in the low replacement

values (Table 2). The exclusive groups for each

ecosystem are highlighted in Table 1.

Nitidulidae, Phoridae, Sciaridae, Smin-

thuridae and Termitidae groups with field

capacity, temperature, and fine textural frac-

tions, and the Entomobryidae and Staphylini-

dae families with the pH.

Trophic guilds and biomass: The phy-

tophagous guild, including the groups of defo-

liators, cutters, suckers and miners, was the

most abundant in the three ecosystems and

in all the strata, followed by the predatory,

blood-sucking and saprophagous groups (Fig.

4A). The proportion of trophic guilds had a

greater abundance of phytophagous, predator,

and hematophagous groups in the strata of the

casmophytic savanna and the lithophytic forest,

and of the phytophagous, saprophagous and

predatory groups in the xerophytic scrub.

Although the phytophagous guilds were

the most abundant in all ecosystems, the high-

est biomass especially in the savanna and scrub

ecosystems comes from the polyphagous habit

groups (Kruskal-Wallis, H = 11.76, P = 0.05).

These groups reach about 40 % of the biomass

in the savannas, more than 60 % in the bushes

and scrub and more than 20 % of the biomass

in the forests (Fig. 4B). The guild is comprised

especially of the most abundant groups such

as Formicidae, Gryllidae and Staphylinidae

in the savanna and scrub ecosystems, and by

the groups such as the Cecidomyiidae, Curcu-

lionidae, Drosophilidae, Formicidae, Fulgori-

dae and Riodinidae in the forest ecosystem.

By stratum, the highest biomass values were

found in the shrub stratum, while the lowest

values were recorded in the edaphic stratum of

all ecosystems.

Body size and coloration: About 60 %

of the 112 groups collected had variations of

mean body sizes due to the capture of more

than one morphospecies, making the number

of groups registered in table 1 increase to 182

and allowing, at the same time, a more detailed

characterization of body size distribution along

the vertical structures of the ecosystems. Thus,

for example, the family Blattidae in the shrub

stratum, had an average size of 5.2 mm in the

casmophytic savannas and 6.0 mm for the

xerophytic shrubs; and two forms of the fam-

ily Apidae in the shrub stratum of the savan-

nas had mean lengths of 4.0 mm and 0.7 mm.

Significant differences were found between the

body lengths of the three ecosystems (Kruskal-

Wallis, H = 11.27, P = 0.05). The largest range

of body sizes was found in the shrub stratum

of the savanna ecosystems where lengths of

up to 45 mm were recorded (Fig. 5A), while

the majority of sizes in the scrub ecosystems

were recorded below 10 mm (Fig. 5B). In the

stratum of all ecosystems, a high percentage of

individuals with body sizes between 2.0 mm

and 4.9 mm was observed, this being the most

frequent range of body lengths at the landscape

level (Fig. 5A, Fig. 5B, Fig. 5C).

The light body colorations that comprise

the white-yellow-cream tones and the dark

black-brown colors are the most frequent in all

the ecosystems. The showy colors in orange

and red or blue and green tones are less fre-

quent and constitute less than 10 % of the body

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Fig. 2. A. Bar-chart analysis, B. similarity of Bray-Curtis, P = 0.91. and C. Correspondence (DCA), Eigenvalues: axis 1 =

0.63, axis 2 = 0.09, for the ecosystems studied in the La Lindosa mountains - Colombia. The number assigned to each group

corresponds to Table 1.

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colors of arthropod fauna at the landscape scale

in all the ecosystems and stratum (Fig. 6A,

Fig. 6B, Fig. 6C). In the case of the xerophytic

scrubs, dark colors are more frequent, followed

by light colors in the lower stratum.

DISCUSSION

Abundance and Diversity: The results

generally show a low diversity typical of this

type of zones derived from Guiana Shield

geological formations and extreme climatic

conditions with mostly sandy soils and little

retained humidity (Gentry, 1982; Hernández

et al., 1992). The low group turnover values

measured by the Wittaker index (aW), showed

a low number of shared groups, so that each

ecosystem showed a very particular faunal

composition that was reflected in the low

similarity values (Halffter & Escurra, 1992).

According to Cornell and Lawton (1992), these

low exchange values between the local fauna

and the regional pool are due to a saturation

of local diversity by competition and predation

that for the study area is related to the large

amount of phytophagous and predator groups.

The number of exclusive groups in each

ecosystem was close to 30 %. These groups

that encompass many species could potentially

include a large number of endemic elements

that are very frequent in these environments

formed historically under critical climatic and

particular geological conditions (Hernández

et al., 1992), so they represent great potential

value to be used in ecological conservation

(Raphael & Molina, 2007). On the other hand,

according to the abundance models, for all

ecosystems there are abundant groups with few

individuals or “singletons” (rare taxa with only

one individual), so that diversity does not only

depend on richness but also on the number of

rare or unique groups found in the community,

and the higher the degree of dominance of a

few groups and the lower abundance of the

majority, the lower the diversity (Novotny

& Basset, 2000). These spatial models are

Fig. 3. Canonical correspondence analysis (CCA) for the physicochemical variables and the groups of the arthropod fauna

of the subsurface layer of the soil in ecosystems of the La Lindosa mountains. Numbers to each group correspond to Table

1. Eigenvalues: Axis 1 = 0.68; Axis 2 = 0.56.

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Fig. 4. A. Percentage of trophic guilds B. and proportion of biomass for functional groups of arthropods in ecosystems of

the La Lindosa mountains - Colombia.

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common in natural communities subjected to

critical environmental conditions (Raphael &

Molina, 2007).

Many of the physiological mechanisms,

especially of insects, are highly dependent

on environmental conditions; humidity and

temperature are the most important deter-

minants for the development and activity of

insects (Basset et al., 2003; Chown & Nicol-

son, 2004). When comparatively evaluating

the richness, abundance and diversity of the

arthropod fauna in the vertical structure of the

different ecosystems of the region, differences

were found especially between the shrub fauna

compared to the lower stratum and the forest

canopy. This could be interpreted as a refuge

effect of the understory in the face of high-

er temperature conditions in the canopy and

the herbaceous stratum. The temperature, the

humidity of the air affected by the solar radia-

tion, and the transpiration of the vegetation

produce microclimatic gradients that induce

the mobility of the arthropods, according to

their physiological tolerance and their habitat

preferences for their feeding, incubation, or the

development of juveniles (Chown & Nicolson,

Fig. 5. Body sizes (left) and size frequency (right) of arthropod fauna in A. The stratum of savanna B. Scrub and C. Forest

ecosystems in the La Lindosa mountains - Colombia.

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2004). Temperature is closely related to most

metabolic processes and complex physiologi-

cal triggers that affect population dynamics in

aspects such as metamorphosis and longevity

(Chown & Nicolson, 2004). For the edaphic

stratum, some variables closely related to the

presence or abundance of some groups were

identified with similar results to other studies

already carried out in Colombia, such as the

case of the relationships found between loamy

textured soils with the highest abundance of

the Acari, Phoridae, Sciaridae and Sminthuri-

dae groups and of the relationship of pH to

the Entomobryidae and Staphylinidae families

(Camero & Chammorro, 2021).

Trophic guilds and biomass: The phy-

tophagous guild was the most abundant in all

the ecosystems studied and in all the strata.

This guild also included many groups of arthro-

pod polyphagous habits that take advantage

of plant resources in their adult or immature

forms, as well as at some stage of develop-

ment in their life cycle (Johnson & Triplehorn,

2005). The phytophagous habits include many

groups of arthropods, especially insects that

specialize or take advantage of all plant tissues

in a generalized way and are made up of groups

of folivorous, chopping, sucking, mining, and

sipping habits (Chown & Nicolson, 2004;

Price, 1984). Under conditions of great climatic

demand, such as in the case of the Sierra de La

Lindosa mountain range, it is more common to

find a greater abundance of generalist groups

than specialized ones. These obtain the maxi-

mum benefits of hydration from the consump-

tion of leaf structures and conducting tissues

(Novotny et al., 2002).

Herbivory is the most important process

in the transformation and the energy flow of

ecosystems, quantifiable in the biomass of

herbivorous fauna that assimilates around 20

% of the most palatable plant organs, either

from surface tissues of exposed organs or their

internal fluids (Del Val, 2012; Price, 1984). In

natural ecosystems, most herbivorous insects

are included especially within the orders

Hymenoptera, Lepidoptera, Coleoptera, Dip-

tera, Hemiptera and Orthoptera, whose energy

and accumulated biomass is used by predatory

and parasitic groups (Del Val, 2012). Predatory

and parasitic groups represented in the ecosys-

tems studied in the Sierra de La Lindosa are

the groups Acari, Araneae, Ceratopogonidae,

Chalcididae, Culicidae, Dolichopodidae, Gryl-

lotalpidae, Mantidae, Pselaphidae, Rhangioni-

dae, Scydmaenidae, Tachinidae and Vespidae.

Fig. 6. Proportion of body color in the different stratum of the A. Savanna B. Scrub and C. Forest ecosystems in the La

Lindosa mountains - Colombia.

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The highest values of the total biomass

were found in the scrub ecosystem where the

greatest abundance of groups was found, fol-

lowed by the biomass values of the savannas

that at the same time had the highest groups

richness. Biomass, then, depends more on the

number of individuals than on the richness

or diversity. In the savanna ecosystem, the

largest body sizes were found but with little

abundance, while the intermediate sizes of the

groups collected in the bushes had a greater

number of individuals. On the other hand, the

direct incidence of solar radiation on ecosys-

tems with an absence of arboreal vegetation

requires greater mechanisms of tolerance for

fauna to high temperatures. These faunal adap-

tations to the conditions of greater environmen-

tal demand, should tend to reduce the loss of

body water and climate tolerance by reducing

the surface/volume ratio (Danks, 2007).

In the herbaceous and edaphic stratum, the

transformation of biomass is carried out espe-

cially by the groups that make up the saproph-

agous, coprophagous, xylophagous, and

fungivorous guilds that contribute to nutrient

release following the detrital pathway (Cole-

man & Wall, 2015; Odum & Barret, 2006). In

the ecosystems of the study area, the biomass

of these detritivore guilds represents around 20

% of the total biomass of the arthropod fauna

of the lower stratum, and they are made up

of the groups Anthophoridae, Entomobryidae,

Labiduridae, Labiidae, Isopteridae, Muscidae,

Mycetophilidae, Onychiuridae, Phoridae, Pti-

liidae, Scarabaeidae, Sciaridae, Scolytidae,

Sminthuridae, Sphaeroceridae, Sphecidae,

Stratiomyidae, Tephritidae and Termitidae.

Most of these groups permanently perform

their ecological functions in these strata, but

many others only perform temporary functions

in some of their stages of development (Cole-

man & Wall, 2015).

Body size and coloration: Body length is

a variable generally closely related to environ-

mental conditions (Stork & Blackburn, 1993).

Most of the body sizes of the arthropod fauna

collected in all the vertical stratum of the

study area are between 2.0 mm and 4.9 mm,

followed by a higher frequency of smaller

sizes. Although in all the ecosystems studied

the greatest size variety was found in the shrub

stratum, large body lengths are very rare,

agreeing with Peters (1983) that they are a low

proportion in natural ecosystems. Most of the

sizes smaller than 2.0 mm correspond to groups

that are within the scale of white-yellow-cream

colors, while the sizes above 10 mm that could

be considered as large, are mostly located

within the black-brown color scale.

Large sizes, more frequent in the shrub

stratum, have greater lengths ranging in savan-

na ecosystems (Fig. 5A), with sizes between

9.0 mm and 45.0 mm, corresponding to the

groups Pentatomidae, Chrysopidae, Gryllidae,

Reduviidae, Vespidae, Tettigoniidae, Prosco-

piidae and Mantidae; most of these groups are

colored white-yellow-cream. In the xerophytic

scrub (Fig. 5B), the longest ranges of lengths in

the shrub stratum are between 9.5 mm and 17.0

mm in the Apidae, Mantidae, Asilidae and Rio-

dinidae groups with black-brown colors; and

in the shrub stratum of lithophytic forests (Fig.

5C), the longest ranges are between 10.0 mm

and 25.0 mm in the Cynipidae, Scarabaeidae,

Cydnidae, Blattidae, Vespidae and Riodinidae

groups with a higher frequency of dark colors.

The light colors that are very frequent in the

upper strata allow a greater reflection of the

incident of solar radiation on the arthropods´

surface and is of great value as an evasive

mechanism to high temperatures caused by

direct radiation. The dark tones, more com-

mon in the lower strata of bushes and forests

decrease the activities of organisms and slow

down resource consumption in high direct

radiation environments (Danks, 2007; Forsman

et al., 2008).

Regional characterization of the arthro-

pod fauna: The ecosystems studied were char-

acterized by low diversity values of arthropod

communities, low exchange values, a high

percentage of groups not shared between eco-

systems and are made up of a particular faunal

richness that responds to local microclimatic

factors. The greater abundances were found in

the intermediate strata where trophic structures

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are represented with a greater proportion of

groups of phytophagous habits, body sizes

between 2.0 and 5.0 mm and a predominance

of dark colors. The general trends in length

measurements in the three ecosystems are the

largest means of sizes in the herbaceous stra-

tum and the presence of smaller sizes in the

subsurface soil stratum. The low frequency of

large body sizes could be explained as a general

adaptation of the fauna to climatic demands

that under high temperature conditions favor

small sizes (García-Barros, 2000).

There is a higher incidence of polyphagous

and phytophagous groups in the total biomass

of the ecosystems, and this does not depend on

the presence of large sizes that generally have

low abundances, but rather on the groups with

intermediate sizes with higher abundances. The

detritivore and mycophagous groups are much

more frequent in the surface stratum of the soil

of all ecosystems due to the greater supply of

organic material (Basset et al., 2003).

Regarding vertical stratification and in the

absence of a greater number of autoecological

studies explaining habitat preference, this can

only be interpreted considering the availability

of resources (Basset et al., 2003). The interme-

diate strata (herbaceous and shrubs) contain

greater food offers that are reflected in values

of greater abundance and diversity with respect

to the any other stratum.

Ethics statement: The authors declare that

they all agree with this publication and that

they have made contributions that justify their

authorship; that there is no conflict of interest

of any kind; and that they have complied with

all relevant ethical and legal requirements and

procedures. All funding sources are fully and

clearly detailed in the acknowledgments sec-

tion. The respective signed legal document is

in the journal’s archives.

ACKNOWLEDGMENTS

We thank the Faculty of Sciences and

the Department of Biology of the National

University of Colombia and the community of

San José del Guaviare for making this research

possible and Professor Thomas Defler of the

Department of Biology of the Universidad

Nacional de Colombia for reviewing the trans-

lation of the manuscript.

RESUMEN

Estratificación vertical de artrópodos en ecosistemas

secos de la Guayana colombiana: patrones

morfológicos y sus implicaciones ecológicas.

Introducción: A pesar del interés que despiertan los

ecosistemas derivados de las formaciones guyanesas, se

desconoce la estructura vertical de las comunidades y las

relaciones de la biota con las condiciones climáticas.

Objetivo: Caracterizar la estructura y composición vertical

de la artropofauna asociada a tres de los ecosistemas más

representativos de la zona norte de la serranía de La Lin-

dosa en Colombia, con base en parámetros morfológicos

y ecológicos.

Métodos: Se muestreó la artropofauna, desde el nivel del

suelo subsuperficial hasta los estratos arbustivos y arbó-

reos, y se identificó hasta el nivel de familia o grupo supra-

específico. Se determinaron los valores de diversidad Alfa

y Beta, se realizaron mediciones de la longitud corporal y

se determinó la coloración y el nivel trófico de cada grupo.

Resultados: La composición y diversidad de la artropo-

fauna fue diferente en cada ecosistema y estrato vertical y

la mayoría de los grupos de artrópodos en todos los ecosis-

temas estudiados presentan abundancias bajas. Los grupos

de hábitos fitófagos y depredadores fueron frecuentes en

todos los ecosistemas y la mayor biomasa de artropofauna

proviene de grupos de hábitos polífagos, de tamaño medio

y de gran abundancia. Las coloraciones claras y oscuras

son las más frecuentes a escala de paisaje.

Conclusión: Los ecosistemas estudiados se caracterizan

por los bajos valores de diversidad y recambio y por la

gran cantidad de grupos no compartidos que aparentemente

responden a las características microclimáticas; sin embar-

go, existen algunas generalidades a escala de paisaje como

la mayor riqueza y abundancia de grupos en los estratos

intermedios, la mayor proporción de grupos de hábitos

fitófagos y tallas corporales medianas y el predominio de

coloraciones oscuras en los estratos inferiores.

Palabras clave: artrópodos; estratificación vertical; grupos

funcionales; gremios tróficos; Guyana colombiana.

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