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INSECTS AS INDICATORS OF ENVIRONMENTAL
CHANGING AND POLLUTION: A REVIEW OF
APPROPRIATE SPECIES AND THEIR MONITORING
OS INSETOS INDICADORES DE ALTERAÇÃO E
POLUIÇÃO AMBIENTAL: UMA REVISÃO DAS
ESPÉCIES ADEQUADAS E DO SEU MONITORAMENTO
José Renato Mauricio da Rocha1, Josimar Ribeiro Almeida2,
Gustavo Aveiro Lins3, Alberto Durval4
1Universidade Federal de Mato Grosso - UFMT. Rua. Bento Alexandre dos Santos,
717 Centro. CEP 78.280-000, Mirassol D'Oeste, MT
2UFRJ/Escola Politécnica/Cidade Universitária/bloco D/sala 204/Rio de Janeiro, RJ
3CEDERJ, SEE/RJ, CEDAE. Rua Farias Brito 50/104 - CEP 20540320, Rio de
4Universidade Federal de Mato Grosso - UFMT - Rua 213, Quadra 49, n. 13 setor 2
Bairro Tijucal, CEP 78.088-18,5 Cuiabá, MT.
Responses of some species to disturbances can be used as a parameter of
analysis about levels of change in the environmental services. These species can be
used as environmental bioindicators. Class Insecta has many appropriate species.
This paper aims an analysis of bioindicator species of the impact caused by intensive
agriculture, deforestation, reforestation and pollution of aquatic and terrestrial
Keywords: Bioindicators. Insecta. Environmental polution. Monitoring.
A resposta de algumas espécies animais e vegetais às perturbações pode ser
utilizada como parâmetro de análise quanto aos níveis de alteração do funcionamento
dos serviços ambientais, e por isso são consideradas bioindicadoras das alterações
ambientais. No entanto, algumas espécies respondem mais fidedignamente do que
outras a estas alterações. A classe Insecta possui muitos representantes adequados
para este tipo de análise. Este trabalho objetiva a análise das espécies consideradas
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bioindicadoras das consequências causadas pela agricultura intensiva, pelo
desflorestamento, reflorestamento e pela poluição de ambientes aéreos, aquáticos e
Palavras-chave: Insecta. Bioindicadores. Alteração ambiental. Poluição. Perícia
There was a growing change of natural environments around the world, as a
result of the growth of human population in recent decades. The economic potential
of biodiversity and advanced destruction process of land ecosystems, especially in
tropical regions, led to the search for an extinction rate estimation of plant and animal
species, which are around 27,000 per year (ANDRADE, 1998; CHEY et al., 1997).
Invertebrates are more severely and quickly affected than other taxa by
changes in the landscape. The insects are responsible for many processes in the
ecosystem and its loss can have negative effects on entire communities. Thus, a
strong understanding of insect responses to human activity is necessary both to
support policy decisions for conservation and to evaluate functional consequences of
human disturbance on ecosystems (NICHOLSA et al., 2007).
Studies about biodiversity preservation in ecosystems can provide information
about maintenance of environmental resources and sustainable development. Insects
are the most abundant animals in almost all ecosystems and can be used to evaluate
the impact of environmental change. Through population and behavioral studies and
the taxonomy of species, it’s possible to estimate what the current degradation rate is
and its future consequences. This paper aims to analyze the major groups of insect
indicators on the aquatic and terrestrial environments.
2. ECOSYSTEMS MONITORING WITH BIOINDICATORS SPECIES
Currently, a relevant question is whether fragmented environments can
preserve the diversity and abundance of insect species such as the high degree of
endemism observed in wild areas. In addition to what would be the fragmented
environments consequences on generalist species populations, which are an important
link in the food chain and development of plant species for pollination.
Many arthropods are used for bioindication because: a) the most frequently
collected taxa (such as beetles and spiders) are polyphagous predators and are
considered important for the biological control, b) collections are made easily with
pitfall traps, and c) catches are usually large enough to allow statistical analysis.
According Martos et al. (1997), environmental indicators are quantitative and
qualitative parameters able to show changes in the environment, where physical,
HOLOS Environment, v.10 n.2, 2010 - P. 252
biological, chemical or human phenomena are not studied alone, but together in the
complex dynamics of the environment.
Entomofauna studies to furnish information about ecosystems conservation
status their productivity and levels of water contamination and pollution. Therefore,
bioindicator species identification is essential, due to the important role that these
organisms have as transformers and regulators of ecosystems (BROWN, 1991;
CAMERO and CHAMORRO, 1995 apud RUBIO, 1999).
Concern with environmental issues has raised the demand for bioindicators
able to reflect their environment. Among these organisms, the insects may contribute
to a practical assessment of the sustainability degree (LOPES, 2008). According
Tylianakis et al. (2004), indicator insects become particularly useful because they
represent more than half of all species and their diversity allow assessing the
difference between habitats on acceptable refined scale. Insect groups used as
environmental bioindicators should have the characteristics shown in the Table 1.
Table 1 - Insect groups characteristics used as environmental indicators
Richness and species diversity Four in five species of animals are insects
Most species require few efforts for their
capture, except toxic species.
The small size of samples helps to their
capture and transport;
Many species may have low tolerance to
abiotic factors, which allows to link
certain insect groups with certain
Fragility to small changes
It allows to select demographical or
behavioral variables that can be
measured or observed in the field, and
have a close correlation with the pre‐
selected abiotic variables;
Organism’s responses To identify levels of environmental
Modified from Andrade (1998); Peck et al. (1998).
Requirements for aquatic insects groups to be considered environmental
quality bioindicators differ slightly from the characteristics attributed to bioindicators
in land environments. According to Peck et al. (1998), the bioindicators are: a)
Respond quickly to environmental changes; b) Have few generations per year; c) Are
easily sampled and identified; d) Show high sensitivity for detecting early changes in
their geographical area; e) Provide information without interruption of the extent
damage caused by environment alteration or pollution.
Some taxonomical and sampling difficulties have restricted the use of several
species of Coleoptera (beetles) and Homoptera (bugs) Orders as environmental
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bioindicators, especially in the tropical region (HOLOWAY, 1983 apud CHEY et al.,
1997). These concerns were also demonstrated by Carlton and Robison (1998) with
subfamily Aleocharinae (Coleoptera: Staphylinidae) due to the large number of
undescribed taxa and the lack of reliability on those already described. Moreover,
Frouz (1999) reported as one of the disadvantage to the use of Diptera species (flies),
as environmental bioindicators, the great taxonomic difficulty, especially in their
3. BIOINDICATOR INSECT GROUPS
Several aquatic insects groups can be used as aquatic environment
bioindicators (Table 2). Odonata (dragonflies) species are very sensitive to changes
caused to their habitat, especially lakes and flooded drainage areas (CORBET, 1980).
Hamilton and Saether (1971) and Hardersen (2000) reported the potential of aquatic
insects as indicators of water quality. Several other species of the families Gyrinidae,
Dytiscidae, Hydrophilidae (Coleoptera), Notonectidae, Veliidae (Heteroptera) and
Plecoptera and Ephemeroptera Orders have high adaptive capacity, colonizing most
of the environments and occurring throughout the year, reflecting ecological and
geographical changes, and hence their conservation status.
The tolerance of aquatic organisms to heavy metals has been explained by the
metallothioneins (MTs) formation in many aquatic organisms. If the presence of MTs
is a measure of metal tolerance, the measurement of MTs could provide clues about
the tolerance in this organisms and possible toxic agents responsible for
environmental stress (BISTHOVEN et al., 1998). However, insects are less used as
pollution bioindicators by metals, although species of the genus Halobates are
suitable for bioindication of cadmium and mercury (NUMMELIN et al., 2007).
Land insects are good bioindicators in various types of environmental change
(Table 2). The Order Coleoptera represents approximately 20% of the total diversity
of arthropods and plays roles in maintaining soil quality, population regulation of
other invertebrates and energy flow, and contributes to the physical and chemistry
soil formation (CARLTON and ROBISON, 1998). Nummelin and Hanski (1989),
Nestel et al. (1993), Louzada and Lopes (1997) and Davis (2000) confirm beetles
species (Coleoptera: Scarabaeidae) have a high potential as environmental indicators
in forest area or agricultural crops.
Beetles from Order Coleoptera and Family Carabidae are important predators.
They participate of biological control, biological monitoring of pollution from oil,
sulfur, herbicides, CO2, insecticides and radioactive phosphorus.
The moths and butterflies (Lepidoptera), besides having basic requirements,
have ecological faithfulness in temperate and tropical regions and are very sensitive
to changes in the environment (GILBERT, 1984; ANDRADE, 1998). The habitat
mosaic maintenance that includes primary forests and other changed areas with
different change levels was the strategy suggested by Wood and Gillman (1998) to
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protect Lepidoptera diversity in natural environment management (WOOD and
Some lepidopteran groups are used as environmental pollution indicators by
heavy metals and carbon dioxide (CO2 concentration) in locations close to industrial
areas and even within urban areas. Presence and consequences of copper, iron, nickel,
cadmium, sulfuric acid ions and other substances used in fertilizers were studied with
pupae of different Geometridae and Noctuidae species (HELIÖVAARA and
VÄISÄNEN, 1990), Eriocraniidae populations (KORICHEVA and HAUKIOJA,
1992), cycle duration and newly hatched larval mortality rate from butterflies (Family
Nymphalidae), which feed on plants subjected to high CO2 concentrations (FAJER et
Collembola are primitive insects that influence soil fertility through microbial
activity stimulation, the fungi spore distribution and inhibit fungi and bacteria action
causing diseases in plants (SAUTER and SANTOS, 1991; RUSEK, 1998). They are
very sensitive to changes in the soil and diversity reduction can show us pollution by
heavy metals, pesticides in agricultural soils and soil water acidification by organic
pollutants and waste (RUSEK, 1998).
Ants are used as soil quality bioindicators and have a key role in the recovery
of degraded and reforested areas (MEJER, 1984). This group, which is very sensitive
to human impact, could be used as environmental indicators in different ecosystems
(FOLGARAIT, 1998; PECK et al., 1998). Depending on the degree of the
environmental change, many expert species are extinct of the site, encouraging the
establishment of dominant, aggressive and generalist species, which can be used as
indicators of disturbed habitats (READ, 1996). The ants presented a strong resistance
to pollutants (radioactive and industrial pollutants) that may be because only about
10% of individuals fall outside the nest and exposed to the harmful pollution effects
(PETAL, 1978). Peck et al. (1998) suggest that some ant groups have potential as
biological indicators of soil conditions, crop management and assessment systems for
plantations in agroecosystems. The impact of ants in soil is demonstrated by leaf
cutting ones in the tropics, where they are the most important agent of change in the
soil, contributing to improving physical and chemical quality (CHERRET, 1989).
Order Diptera is a very heterogeneous group and there are some restrictions on
its use as bioindicator because of the lack of ecological knowledge of many groups of
flies. However, some flies species are considered good environmental change
bioindicators. Bartosova et al. (1997) showed the potential of species from the Family
Sarcophagidae as environmental pollution indicators by heavy metals, asbestos fibers
and waste chemicals. However, due to variability in the flies’ sensitivity to
insecticides and herbicides, Frouz (1999) recommends that one must be careful when
using some species of flies as chemical indicators of contaminated soil.
Family Syrphidae, one of the largest families of Diptera, has wide distribution,
well known taxonomy and its larvae require different environmental conditions,
which makes these flies’ good bioindicators. Due to environmental requirements of
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their larvae, these insects are particularly affected by the landscaping diversity
reduction (SOMMAGGIO, 1999).
Most of the research on pollinators as bioindicators have been on population
level and have focused mainly on bees. The pollinator strength and its population size
are generally considered the most important features for plant reproduction,
especially to the agricultural crops (KEVAN, 1999). Pollinators, especially
honeybees (Apis mellifera), are considered reliable biological indicators because they
show environment chemical impairment due to high mortality rate and intercept
particles suspended in air or flowers. These substances can then be detected using
methods of analysis (GHINI et al., 2004).
Table 2 - Bioindicator insect groups from aquatic and land environments and their role in the
Group Common Names Biomonitoring Habitat
Odonata Order dragonflies and damselflies water quality aquatic
predaceous diving beetles
due to high adaptive
due to high adaptive
Halobates ocean‐skaters cadmium and lead aquatic
Scarabaeidae Family beetles in forest and agricultural
Carabidae Family beetles
oil, sufur, herbicide, CO2,
Lepidoptera Order moths and butterflies
heavy metals and CO2
Collembola Order springtails
pollution by heavy metals,
pesticides and water
Formicidae Family ants
degraded and reforested
Sarcophagidae Family flies and mosquitos heavy metals land
Syrphidae Family flies and mosquitos are affected by diversity
Apis mellifera domestic bees chemical environmental
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4. BIOINDICATOR INSECTS IN AGRICULTURAL AND FOREST AREAS
Cultivated areas or reforested areas with some diversity of plant species have
shown high insect species diversity and greater ecological stability, where the
competition for resources is intense, preventing the prevalence of few dominant
species (CHEY et al., 1997; DORVAL, 1995; MEZZOMO et al., 1998).
Explanations for loss of species in agricultural environments are: changes in
microclimatic conditions, foraging activity and nesting locations, reduced food
availability from the use of agrochemicals and interactions with other species (DE
Monoculture is predominant in agricultural areas. In these areas there are many
populations of defoliator and sucking insects, characteristics of unbalanced
environment (ABATE et al, 2000). The use of fertilizers and chemicals is responsible
for the decline of biodiversity in simplified agricultural systems since it eliminates a
large number of insects acting as biological control agents.
Hymenoptera communities are common in agricultural areas. They act as crops
and wild plant pollinators. Furthermore, many species that live in society are
predators or parasitoids, acting as of biological control agents (TYLIANAKIS et al.,
We should consider the adoption of environmentally correct practices in areas
under agricultural management. The aeration depth control could prevent layers
destruction, where the activity of decomposer organisms (Collembola, Coleoptera) is
intense. The rational use of products to soil correction, fertilization and crop residues
incorporation can improve the organic soil part and provide optimal conditions for
decomposer insects and nitrogen fixing bacteria, increasing insect biodiversity.
Nummelin and Hanski (1989), Nestel et al. (1993), Perfecto et al. (1997), Honek and
Jarosik (2000) confirm the importance of cultural diversity for the preservation of the
diverse insect groups characteristic of not much changed areas.
In the forest, the imbalance begins with native vegetation replacement, which
normally has high insect diversity, for homogeneous plantation areas, where
ecological balance is fragile and insect diversity is reduced. Therefore, the number of
harmful insect species is quite high and frequently occurring population booms,
especially of defoliator lepidopteran (DORVAL, 1995).
The reforestation is usually located in nutrient-poor soils, and at certain times
of year the trees are exposed to water stress, becoming highly susceptible to attack by
insects. During this period there may be population booms of aggressive and
Remaining strains of trees selective logging can serve as a host material,
providing favorable conditions for occurrence of dominant Scolytidae species
(ambrosia-beetle) population booms. Moreover, there is the fire that destroys
important soil layers, causing damages and weakening the trees, becoming them
susceptible to attack by insects.
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Therefore, the occurrence of harmful and dominant insect species in
agricultural and forest environments may be environmental imbalance evidences,
caused by changes in biotic and abiotic factors (Table 3).
Table 3 - Difference between agricultural and forest areas during biomonitoring
Agricultural Area Forest Area
defoliator and sucking insects deforestation increases number of harmful
diversity reduced due to fertilizers deforestation decreases insect diversity
pollinators: bees and wasps reforestation occurs in poor soil, increases
water stress and insects attacks
Social species: biological control
remaining strains: host material to ambrosia‐
Fire: destroys soil and trees
5. INSECTS AS BIOINDICATORS OF ENVIRONMENTAL POLLUTION
Many insects can be used as environmental pollution bioindicators (Table 4).
Ants have been used to measure pollutant concentrations in borealis forests and
Australia, and are currently used to monitor disturbed ecosystems. Bees are
considered one of the most versatile and efficient bioindicators. They are used to
monitor trace metals in urban environments, radioactivity after the Chernobyl
disaster, pesticides and herbicides effects, industrial wastes and pollutants (URBINI
et al., 2006).
Many studies have demonstrated deformities in larvae from several genera
from the Family Chironomidae (eg Procladius, Chironomus and Cryptochironomus)
and the results indicate that the abnormalities are strongly associated with polluted
sediments (SERVIA et al., 1998). Gerridae are indicated to detection of different iron
and manganese concentrations, but seem less suitable for nickel and lead
accumulated (NUMMELIN et al., 2007).
Wasps from the Polistes and other social wasps are at the top of the food chain
and, therefore, are exposed to dangerous biological concentration. As its mass larval
fecal can accumulate lead up to 36 times the adult body, these wasps seem to be a
promising species for pollution by lead biomonitoring (URBINI et al., 2006).
Table 4 - Insects groups used as environmental pollution bioindicators
bees trace metals, radioactivity, pesticides, herbicides
and industrial pollutants
ants polluent concentration at Australia
Larvae Family Chironomidae iron and manganese concentration
Genus Polistes (wasps) lead pollution
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6. OTHER BIOINDICATOR INSECT GROUPS
According to Eggleton et al. (1994), termites are important decomposers in
land ecosystems. Its activity increases soil infiltration capacity, leading to water
retention and soil productivity. In forests, they play a role in plant origin material and
organic soil decomposition and incorporation. In agricultural, pasture and
reforestation areas they are not always perceived because its nests are underground,
and their presence is only noticed by the damage they cause to the plants.
Aphids are pollution indicators, because they show an increase in their
population density when feeding on hosts exposed to environments with high CO2
concentrations. However, studies showed no significant correlation between CO2
increase and Homoptera population density (CANNON, 1998).
The use of bioindicators is essential for environmental monitoring. The main
characteristics of a bioindicator are: richness and diversity species, easy handling,
ecological faithfulness, fragility to small environmental changes and good organism
responses. Class Insecta has all of them. However, some species respond better than
others to these changes and according to the environment.
In the aquatic environment, Odonata species are more sensitive to
environmental changes in the water. Coleoptera, Heteroptera, Plecoptera and
Ephemeroptera have high adaptive capacity. In the land, Coleoptera Order has many
bioindicator species, for example Scarabaeidae Family (beetles) in forest and
agricultural cultures. Some Lepidoptera and Diptera groups are used as heavy metal
Agricultural and forestry systems have shown high insect diversity and better
ecological stability in relation to monoculture. The use of fertilizers and chemicals
reduces biodiversity in simplified agricultural areas. In the forest, the imbalance
begins with replacement of native vegetation, in areas of homogeneous plantations.
Therefore, it increases the number of harmful insects, especially defoliator
In environmental pollution, bees are used to monitor trace metals in urban
environments, radioactivity, and pesticide and herbicide effects. Gerridae detect
different iron and manganese concentrations.
Therefore, this study concluded that the Class Insecta has many potential
representatives that can be used as environmental bioindicators, among which are
some species from the Coleoptera, Diptera, Lepidoptera, Hymenoptera, Hemiptera,
Isoptera Orders and others.
HOLOS Environment, v.10 n.2, 2010 - P. 259
ABATE, T.; VAN HUIS, A.; AMPOFO, J.K. O. Pest management strategies in
traditional agriculture: An Africana perspectiva. Ann. Rev. Entono. v. 45, p. 631 –
ANDRADE, M. G. Utilizassem de lãs mariposas como bioindicadoras del tipo de
habitat y su biodiversidad em Colômbia. Rev.Acad.Colomb.Cienc.Exact.Fis.Nat. v.
22, n.84, p. 407–421, 1998.
BARTOSOVA, M., GLOVINOVA, E.; POVOLNY, D. Use of flesh-flies (Diptera,
Sarcophagidae) for ecotoxicological bioindication. Ekol.-Bratislava, v. 16, p. 319-
BISTHOVEN, L. J.; NUYTS, P.; GODDEERIS, B.; OLLEVIER, F. Sublethal
parameters in morphologically deformed Chironomus larvae: clues to understanding
their bioindicator value. Freshwater Biol. v. 39, p. 179–191, 1998.
BROWN, K. Conservation of neotropical environments: Insects as indicators. The
conservation of insects and their habitats. Collins N.J. Thomas. Chap. 14, p. 350-
CANNON, R. J. C. The implications of predicted climate change for insect pests in
the UK, with emphasis on non-indigenous species. Global Change Biol.. v. 4, p.756-
CARLTON, C. E.; ROBISON, H. W. Diversity of litter-dwelling beetles in the
Ouachita Highlands of Arkansas, USA (Insecta:Coleoptera). Biodivers. Conserv., v.
7, p. 1589–1605, 1998.
CHERRET, J. M. Leaf-cutting ants. Biogeographical and ecological studies.
Ecosystem of the World, Tropical Rain Forest Ecossystem, p. 473-488, 1989.
CHEY, V. K.; HOLLOWAY, J. D.; SPEIGHT, M. R. Diversity of moths in forest
plantations and natural forests in Sabah. Bull. Entomol. Res. v. 87, p. 371- 85, 1997.
CORBET, P.S. Biology of Odonata. Ann. Rev. Entomol. v. 25, p. 189-217, 1980.
DAVIS, A. Does reduced-impact logging help preserve biodiversity in tropical
rainforest? A case study from Borneo using dung beetles (Coleoptera: Scarabaeoidea)
as indicators. Environ. Entomol., v. 29, n.3, p. 469-73, 2000.
DE BRUYN, L.A.L. Ants as bioindicators of soil function in rural environments.
Agr. Ecosyst. Environ. v. 74, p. 425–441, 1999.
HOLOS Environment, v.10 n.2, 2010 - P. 260
DORVAL, A. Análise faunística e flutuação populacional de lepidópteros em
Eucalyptus urophylla e Eucalyptus cloeziana em Montes Claros, MG.1995. 129
f. Dissertação (Mestrado em Entomologia) – Departamento de Biologia Animal,
Universidade Federal de Viçosa. Viçosa. 1995.
EGGLETON, P.; WILLIAMS, P. H.; GASTON, K. J. Explaining global termite
diversity: productivity or history? Biodivers. Conserv., v. 3, p.318–330, 1994.
FAJER, E. D.; BOWERS M. D.; BAZZAZ, F. A. The effects of enriched carbon
dioxide atmospheres on plant-insect herbivore interactions. Science, v. 243, p.1198–
FOLGARAIT, P. J. Ant biodiversity and its relationship to ecosystem functioning: a
review. Biodivers. Conserv.,, v. 7, p. 1221–1244, 1998.
FROUZ, J. Use of soil dwelling Díptera (Insecta, Díptera) as bioindicaors: a review
of ecological requeriments and response to disturbance. Agr. Ecosyst. Environ., v.
74, p. 167–186, 1999.
GILBERT, L. E. The biology of butterfly communities. The biology of butterfly, p.
41 – 54, 1984.
GHINI, S.; FERNÁNDEZ, M.; PICÓ, Y.; MARÍN, R.; FINI, F.; MAÑES, J.;
GIROTTI, S. Occurrence and distribution of pesticides in the province of Bologna,
Italy, using honeybees as bioindicators. Arch. Environ. Contam.Toxicol., v. 47, p.
HAMILTON, A. L.; SAETHER, O. A. The occurrence of caracteristc deformities in
the chiromomid larvae of several Canadian lakes. The Canad. Entomolog., v. 103,
p. 363 – 68, 1971.
HARDERSEN, S. The role of behavioural ecology of damselflies in the use of
fluctuating asymmetry as a bioindicator of water poppution. Ecolog. Entomol., v. 25,
p. 45 – 53. 2000.
HELIÖVAARA, K.; VÄISÄNEN, R. Heavy-metal contents in pupae of Bupalus
piniarus (Lepidoptera: Geometridae) and Panolis flammea (Lepidoptera: Noctuidae)
near an industrial source. Environ. Entomol., v. 19, p. 481 – 485, 1990.
HONEK, A.; JAROSIK, V. The role of crop density, seed and aphid presence in
diversification of field communities of Carabidae (Coleoptera). Eur. J. Entomol. v.
97, p. 517 – 525, 2000.
HOLOS Environment, v.10 n.2, 2010 - P. 261
KEVAN, P. G. Pollinators as bioindicators of the state of the environment: species,
activity and diversity. Agr. Ecosyst. Environ., v. 74, p. 373 – 393, 1999.
KORICHEVA, J.; HAUKIOJA, E. Effects of air pollution on host plant quality,
individual performance, and population density of Eriocrania miner (Lepidoptera:
Eriocraniidae). Environ. Entomol., v. 26 (6), p. 1386 – 1392, 1992.
LOPES, B. G. C. Levantamento da entomofauna bioindicadora da qualidade
ambiental em diferentes áreas do Alto Jequitinhonha – Minas Gerais. 2008. 47f.
Trabalho de Conclusão de Curso - Escola Agrotécnica Federal de Inconfidentes.
Inconfidentes, Minas Gerais. 2008.
LOUZADA, J. N. C.; LOPES, F. S. A comunidade de Scarabaeidae copro-necrófagos
(Coleoptera) de um fragmento de Mata Atlântica. Rev. Brasil. Entomol., v. 41, n.1,
p. 117–121, 1997.
MARTOS, H. L.; MAIA, N. B.; BROWN-Jr., S. Indicadores Ambientais. Sorocaba,
USP, 266p, 1997.
MEJER, J. D. The influence of ants on seeding operations in Northern Australian
mined areas. Reclam. Reveg. Res. v. 2, p. 299 – 313, 1984.
MEZZOMO, J. A.; ZANUNCIO, J. C.; BARCELOS, J. A.V. ; GUEDES, R. N. C.
Influência de faixas de vegetação nativa sobre Coleoptera em Eucalyptus cloeziana.
Rev. Árvore, v. 22, n. 1, p. 77 – 87, 1998.
NESTEL, D.; DICKSCHEN, F.; ALTIERI, M. A. Diversity patterns of soil macro-
coleoptera in Mexican shaded and unshaded coffee Agroecosystems: an implication
of habitat pertubation. Biodivers. Conserv., v. 2, p. 70 – 78, 1993.
NICHOLSA, E.; LARSENB, T.; SPECTORA, S.; DAVISE, A. L.; ESCOBARC, F.;
FAVILAD, M.; VULINECE, K. Global dung beetle response to tropical forest
modification and fragmentation: A quantitative literature review and meta-analysis.
Biologic. Conserv.. v. 137, p. 1– 19, 2007.
NUMMELIN, M.; HANSKI, I. Dung beetles of the Kibale Forest, Uganda;
Comparison between virgin and managed forest. J. Trop. Ecol, v. 5, p. 349 – 352.
NUMMELIN, M.; LODENIUS, M.; TULISALO, E.; HIRVONEN, H.; ALANKO, T.
Predatory insects as bioindicators of heavy metal pollution. Environ. Pollut., v. 145,
p. 339–347, 2007.
PECK, S. L.; MCQUAID, B.; CAMPBELL, C. L. Using ant species (Hymenoptera:
HOLOS Environment, v.10 n.2, 2010 - P. 262
Formicidae) as a biological indicator of agroecosystem condition. Environ.
Entomol., v. 27, n.5, p. 1102–1110, 1998.
PERFECTO, I.; VANDERMEER, J.; HANSON, P.; CARTÍN, V. Artrhopod
biodiversity loss and the transformation of tropical agro-ecosystem. Biodivers.
Conserv., v. 6, p. 935– 945. 1997.
PETAL, J. Adaptation of ants to Industrial Pollution. Memorabilia Zool., v. 29, p. 99
- 108, 1978.
READ, J. L. Use of ants to monitor environmental impacts of salt spray from a mine
in arid Austrália. Biodivers. Conserv., v. 5, v.12, p. 1533–1543, 1996.
RUBIO, C. E. Estudio comparativo de la fauna de coleópteros (Insecta: Coleoptera)
en dos ambientes de bosque húmedo tropical colombiano. Rev Colomb. Entomol., v.
25 (3-4), p. 131 – 135, 1999.
RUSEK, J. Biodiversity of Collembola and their functional role in the ecosystem.
Biodivers. Conserv., v. 7, p. 1207 – 1219, 1998.
SAUTTER, K. D.; SANTOS, H. R. Insetos bioindicadores na recuperação do solo.
Ciênc. Hoje, 1991.
SERVIA, M. J.; COBO, F.; GONZÁLEZ, M. A. Deformities in larval Prodiamesa
olivacea (Meigen, 1818) (Diptera, Chironomidae) and their use as bioindicators of
toxic sediment stress. Hydrobiol., v. 385, p. 153 – 162, 1998.
SOMMAGGIO, D. Syrphidae: can they be used as environmental bioindicators? Agr.
Ecosyst. Environ., v. 74, p. 343– 356, 1999.
TYLIANAKIS, J.; VEDDELER, D.; LOZADA, T.; LÓPEZ, R. M.; BENÍTEZ, P.;
KLEIN, A. M.; KONING, G. H. J.; OLSCHEWSKI, R.; VELDKAMP, E.;
NAVARRETE, H.; ONORE, G.; TSCHARNTKE, T. Biodiversity of land-use
systems in coastal Ecuador and bioindication using trap-nesting bees, wasps, and
their natural enemies. Lyonia. v. 6, n. 2, p.7–15, 2004.
URBINI, A.; SPARVOLI, E.; TURILLAZZI, S. Social paper wasps as bioindicators:
a preliminary research with Polistes dominulus (Hymenoptera: Vespidae) as a trace
metal accumulator. Chemosph. v. 64, p. 697–703, 2006.
WOOD, B.; GILLMAN, M. P. The effects of disturbance on forest butterflies using
two methods of sampling in Trinidad. Biodivers. Conserv., v. 7, p.597– 616, 1998.
Manuscrito recebido em: 10/03/2008
Revisado e Aceito em: 22/12/2010