Hodkinson Jackson 2005

DOI: 10.
1007/s00267-004-0211-x
Terrestrial and Aquatic Invertebrates as Bioindicators

for Environmental Monitoring, with Particular
Reference to Mountain Ecosystems
IAN D. HODKINSON is reviewed and critically evaluated. Their suitability and
School of Biological and Earth Sciences value for assessing a range of environmental problems from
Liverpool John Moores University, Byrom Street pollution impacts, through habitat evaluation for conserva-
Liverpool, L3, AF, UK tion to the long-term degradation and recovery of ecosys-
tems, is critically discussed. Guidelines are provided for the
JOHN K. JACKSON
choice of appropriate bioindicators. Examples of the use of a
Stroud Water Research Center
broad spectrum of invertebrates to assess a variety of
970 Spencer Road environmental problems are summarized. The particular
Avondale, Pennsylvania 19382, USA
potential of invertebrates for monitoring montane ecosys-
tems is highlighted.
ABSTRACT / The use of terrestrial and aquatic invertebrates
as a management tool for monitoring change in ecosystems
A bioindicator can be defined as ‘‘a species or group nition of this connection, and the need to protect
of species that readily reflects the abiotic or biotic state human health and recreation, fisheries production,
of an environment, represents the impact of environ- and industrial/agricultural systems, led to the early
mental change on a habitat, community, or ecosystem, development of water quality regulations and moni-
or is indicative of the diversity of a subset of taxa, or of toring methods. Early efforts include river and stream
the wholesale diversity, within an area’’ (McGeoch eutrophication typology (Sprobiensystem of Kolkwitz
1998). The principles and ranges of applications for and Marsson 1909) and lake eutrophication typology
the use of invertebrate bioindicators as tools for envi- (Thienemann 1921). The utility of invertebrates for
ronmental management within mountain environ- assessing environmental conditions in aquatic ecosys-
ments are similar to those pertaining generally. This tems has thus long been recognized (Cairns and Pratt
paper focuses primarily, therefore, on the common 1993), and this has spawned a variety of biological
problems and issues arising from the use of aquatic monitoring tools that use aquatic invertebrates
(i.e., freshwater) and terrestrial invertebrates as bioin- (Hellawell 1986, Rosenberg and Resh 1993). These
dicators before suggesting some more specific uses monitoring methods recognized that different inver-
within mountain environments. The ideas presented tebrate taxa tolerate organic pollution to a lesser or
originate from an international workshop (Global greater extent and that their differing responses can be
Mountain Biodiversity Assessment–DIVERSITAS pro- used to indicate water quality. For example, in rivers,
gramme) organized by the Austrian Academy of Sci- invertebrate groups such as larvae of Plecoptera and
ences to review critically the range of options for Ephemeroptera were shown to be pollution intolerant,
monitoring long-term impacts of environmental whereas other taxa, such as tubificid worms and par-
change in mountain habitats using invertebrates and to ticular species of chironomid midge larvae, survived
provide realistic guidelines for their use. under deoxygenated conditions verging on anoxia.
There is a strong relationship between human Modern assessment protocols still rely on such indica-
activities and disturbance of the environment. Recog- tor species or assemblages and detailed knowledge of
pollution responses, but they now also often involve
sophisticated transformation or statistical analyses of
KEY WORDS: Bioindication; Indicator species; Pollution; Habitat
degradation; Habitat quality
data. Protocols continue to be developed and refined,
especially for wetland and large river invertebrates.
Published online May 17, 2005 Aquatic invertebrates have, therefore, repeatedly
*Author to whom correspondence should be addressed; email: shown their utility in evaluating aquatic resources. The
[email protected] beauty of this approach is the ease with which it can be
Environmental Management Vol. 35, No. 5, pp. 649–666 ª 2005 Springer Science+Business Media, Inc.
650 I. D. Hodkinson and J. K. Jackson
applied and communicated, and the responsiveness of indicated by changes in the whole invertebrate com-
the indicator invertebrates. munity. It is a question of choosing the right indicators
By contrast, Rosenberg and others (1986) noted for each specific purpose. This necessitates that the
that the effective use of invertebrates in monitoring initial problem be clearly delineated and defined, that
and assessment of the terrestrial environment was less suitable bioindicator organisms be selected using rig-
developed than for aquatic environments, and this still orous criteria, and that the predicted response of the
appears to be the case almost 20 years later. It is not bioindicator taxa be clear and well tested (McGeoch
clear, however, why this difference developed, but a 1998, Pearson 1994). Because knowledge for individual
key factor may be the absence of specific regulations species and species assemblages is often incomplete,
for terrestrial environments, and the lesser need to and environmental stress often involves several con-
assess compliance. In any event, the utility of terrestrial current factors at varying levels, monitoring programs
invertebrates as bioindicators will presumably come to frequently rely on the responses of more than one
match that of aquatic invertebrates in future because indicator to increase the accuracy of their assessments.
terrestrial invertebrates exhibit many of the charac-
teristics that make aquatic invertebrates such valuable The Individual Animal Level Response
bioindicators. Individual animals may serve as short-term bioindi-
The concept of bioindication has, within the past 25 cators of particular environmental conditions, where a
years, been broadened and expanded to address response to a particular environmental stress can be
emerging ecological issues related to conservation demonstrated in their physiology or behavior. For
assessment and landscape management. A plethora of example, in stream-dwelling mayflies and stoneflies,
papers has suggested how an increasingly wide range of the rate of respiration (physiology) fails to compensate
invertebrates might be used to indicate environmental for falling oxygen levels within the water, and this may
trends, impacts, and change or the ecological value of be coupled with more rapid movement of body parts
sites (see Rosenberg and Resh 1993, Dallinger 1994, involved with gas exchange (behavior) (Eriksen and
Paoletti and Bressan 1996, van Straalen 1998, Jonsson others 1996). Similarly, some aquatic midge larvae
and Jonsell 1999, Cortet and others 1999, Moritz and display avoidance behavior when confronted with sed-
others 2001, Reyers and others 2000, Norden and Ap- iments contaminated by heavy metals above certain
pelqvist 2001, Taylor and Doran 2001, Mac Nally and concentrations. Other examples include the bioaccu-
others 2002 for summaries). Many of the suggestions mulation of toxins (e.g., Kovats and Ciborowski 1989,
are vague, impractical, or unworkable and little energy Cain and others 1992, Standley and Sweeney 1995),
has been invested in evaluating, defining, and testing development of biomarkers (e.g., Maycock and others
their appropriateness and applicability as workable bi- 2003), or morphological deformities (fluctuating
oindicator systems. asymmetry or FA). FA refers to the phenomenon that
The purpose of this paper, therefore, is to 1) when some animals are subjected to environmental
examine how and which invertebrates might prove stresses, they show increased levels of asymmetry in
useful as bioindicators, 2) identify criteria for the their body shape and size, usually measured either side
selection of useful bioindicator systems, and 3) evalu- of a bilateral line. The distortion can be measured
ate the use of these systems across a wide range of quantitatively and expressed as an index for a species
potential applications, particularly within montane population. This index may increase with increasing
environments. stress levels and thus serve as a simple way in which to
monitor the impact of a wide range of known envi-
ronmental stress factors. The concept of FA has been
How Can Invertebrates Be Used as Indicators?
widely applied as a stress indicator in both aquatic and
Invertebrates can indicate changes in the environ- terrestrial ecosystems (e.g., Clarke 1993, Lenat 1993,
ment through their responses at different levels of Rabitsch 1997, Groenendijk and others 1998, Tessier
organization, ranging from the individual animal to and others 2000) involving pollution by pesticides,
the total invertebrate community. The appropriateness fertilizers, PCBs, aluminum, heavy metals, and thermal
of the level chosen to indicate a changing environment stress, but with varying degrees of success.
depends on the particular factor(s) that are thought to
be acting. Responses to single pollutants may be picked The Species Population-Level Response
up by changes in individual animals or species popu- Responses here involve changes that are apparent
lations, whereas long-term forest degradation, or the only when observing multiple individuals (popula-
conservation value of particular sites, may be better tions) of single species in response to an external fac-
Invertebrates as Bioindicators 651
tor. Such factors may induce changes in population species. These important species may be Keystone
density as a result of effects on invertebrate perfor- species, in the ecological sense, that is, species having
mance that enhance or reduce rates of recruitment/ several other species depending upon them for their
mortality. There may also be changes in the ‘‘quality’’ existence and where removing them would instantly
of the individual animals, either in the short term eradicate several other species (Mills and others 1993).
through detrimental impacts on growth and develop- The important species may also include rare, relict,
ment (see later) or in the long term through genetic endemic, or endangered taxa of conservation signifi-
selection (Frati and others 1992). Species-level re- cance.
sponses are most easy to interpret when they are linked Invertebrates within any given habitat are generally
to single clearly defined factors, particularly physical or taxonomically diverse, and it may be unrealistic to ex-
chemical features of their environment. The distribu- pect the simple bioindicator organism–environmental
tion of particular monophagous species of herbivorous factor relationships that are observed at the species
insect on their host plants, for example, serves as a level to be repeated at the community level. Because of
sensitive indicator of changing environmental tem- the sheer number of species present, it becomes
peratures (Hodkinson and Bird 1998). Insects shift increasing difficult to establish precise and well-
their distribution relatively rapidly within the broader understood causal relationships between external fac-
geographical range of their plant, and this is most tors and the composition of entire communities.
readily observed among arctic/alpine species along Community composition is thus more usually used to
latitudinal or altitudinal gradients that serve as proxies bioindicate broader aspects of habitat quality and more
for a changing climate (Whittaker and Tribe 1996, general changes within the habitat such as degradation
Randall 1982). Similarly, among soil animals, certain and recovery following stress or disturbance. Never-
earthworm species, particularly Lumbricus spp., are theless, examples of the effective use of whole inver-
good bioindicators of soil pH and several soil arthro- tebrate communities for biomonitoring do exist. The
pods, particularly Collembola, snails and isopod spe- relatively easy-to-sample and species-poor (50–100
cies are known to suffer mortality at known threshold species are commonly collected in a single visit to a
levels of soil contaminants, especially heavy metals unimpaired site) communities of running water eco-
(Cortet and others 1999, van Straalen 1998). Popula- systems, for example, are reasonably well understood
tion genetic structure of mayflies (Benton and Gutt- and the predictable response of the whole community
man 1990), caddisflies (Benton and Guttman 1992), to organic pollution, as mentioned earlier, forms the
and amphipods (Duan and others 2000) have been basis of water quality assessment. More frequently,
observed to change in response to heavy metal expo- however, it is necessary to work with subsets of taxa that
sure. Here the direct linkage between the bioindicator can be shown to act as proxies for the whole commu-
species population and the strength of the external nity. For example, in running water ecosystems, the
factor is recognized and exploited. subset of Ephemeroptera, Plecoptera, and Trichoptera
are commonly monitored together as a single richness
The Community-Level Response variable–EPT Index (Resh and Jackson 1993). To-
Monitoring community-level responses is complex gether, this represents a group that can be identified
in that it involves integrating the responses of numer- reliably, is ecologically important, and contains many
ous species populations. However, the community re- pollution-sensitive species. This subset reflects a com-
sponse provides a valuable perspective with regard to mon response to pollution observed over many years of
the biological magnitude of changes. There is gener- monitoring, and excludes some of the more taxo-
ally little question that a community response is sig- nomically challenging groups (i.e., chironomid midges
nificant because it reflects changes for multiple and oligochaete worms).
species, whereas indicator species responses involve This is clearly the point at which problems can arise.
only one species, and many other species are poten- How representative is the chosen subset? How does
tially unaffected. In addition, in a world with complex one know? Choice of the species subset can be based
sources of disturbance, the multispecies approach on some combination of taxonomic or functional
makes use of more biological monitoring tools (i.e., group criteria as well as responses to disturbance.
species). Manageable taxonomic subsets, which may embrace
Communities possess several attributes useful for genera, families, or higher groupings, should ideally be
bioindication. These include the number of species chosen on the basis that they are representative of the
present (species richness), the relative abundances of whole community and the group can be shown to re-
the different species, and the presence of ‘‘important’’ spond sensitively to the factor affecting the whole
community. Often, however, individual taxonomic others 1999, Carlisle and Clements 1999). However, an
specialists promote the virtues of their own particular alternative approach is being actively explored that
specialist group with scant regard to cross-referencing combines food and feeding habits with a wide variety of
their findings to the residual taxa. A single experi- other biological traits such as body size, fecundity,
mental demonstration of a negative impact of a dis- voltinism, development time, and vagility to describe
turbance on a given taxon does not necessarily make functional community structure relative to a habitat
that taxon a reliable indicator. A consistent, repeatable template (Poff 1997, Statzner and others 2004). This
response to that disturbance is necessary to establish approach shows better promise for detecting changes
the efficacy of the taxon as a bioindicator. The prob- in community structure in response to habitat modifi-
lems may be compounded by the fact that there is of- cation and pollution (Charvet and others 1998, 2000,
ten little consistency in the measured responses by two Dolédec and others 1999, Gayrud and others 2003).
different taxonomic groups to the same external factor One of the problems of using invertebrate com-
(e.g., Heino and others 2003b). In other instances, munities or guilds as bioindicators is that such assem-
however, similar responses are observed in taxonomi- blages are subject to natural stochastic variation in
cally divergent groups such as birds and butterflies addition to the independent deterministic changes
(Blair 1999). Passy and others (2004) observed gener- resulting from pollution or disturbance, particularly
ally similar responses among fish, macroinvertebrates, over the long term. It may be necessary, therefore, to
and algae across numerous streams, but suggested that establish the natural range of variation for the indica-
each taxonomic group responds to a distinct combi- tor community before its use in bioindication: good
nation of environmental factors. Sometimes relation- bioindicators will respond more sensitively to the
ships can be counterintuitive, such as the inverse deterministic forces than to the stochastic ones.
relationship between species richness of gall-forming
insects and plant diversity in tropical rain forest (Cue-
What Can Invertebrates Bioindicate?
vas-Reyes and others 2003). These problems may be
particularly acute where invertebrates are being used to McGeoch (1998) divided bioindicators into envi-
indicate the conservation value of natural habitats or to ronmental indicators (changes in physicochemical
indicate longer-term changes occurring within those environment), ecological indicators (impacts of factors
habitats. The value of particular groups can, however, on ecosystems), and biodiversity indicators (habitat
be enhanced by a knowledge of the habitat fidelity and assessment for conservation). This framework is, how-
specificity of the member species, which aid interpre- ever, a little fuzzy with some conceptual overlap be-
tation and prediction (McGeoch and others 2002). tween categories, and here we have categorized instead
One possible way around this problem of varying the impacting factors or the habitat properties rather
responses within taxonomic groupings is to use se- than their bioindicators. Broadly speaking, bioindica-
lected functional groups or guilds of organisms rather tors can be used to indicate 1) a changing physical
than taxonomic entities (Rawer-Jost and others 2000). environment; 2) a changing chemical environment,
A functional group or guild is defined as a set of particularly with respect to various forms of pollution;
taxonomically unrelated species that perform similar 3) the comparative quality or conservation value of
functions within the community (Simberloff and Da- habitat; and 4) changes in the ecological status of the
yan 1991). This, if used in a targeted manner, can focus habitat with respect to time and place. These may (1, 2,
the effect of an external factor onto an ecological 4) or may not (3 and sometimes 4) involve external
process and those species that are most likely to re- impacts on the habitat.
spond to it. Examples might include the response of
lichen-feeding invertebrates to sulfur dioxide pollution Changing Physical Environment
(acidification) or soil fungus-feeding communities Relative to studies on the chemical environment,
responding to changes in the quality and quantity studies on the physical environment in terrestrial
of available leaf litter after ecosystem disturbance habitats are few, mainly investigating responses to
(decomposition). However, in a biomonitoring study temperature. The response to a changing physical
of anthropogenic disturbance in tropical forests, environment embraces raised or lowered environ-
broad-feeding guilds were weaker discriminators than mental temperatures (mean, range, and frequency of
selected-target taxa within the guild (Basset and others extremes) and patterns of precipitation and drought,
2004). Similarly, biometrics describing trophic or together with associated phenomena such as the fre-
feeding functional structure have not been strong quency of freeze–thaw cycles and the persistence of
indicators for stream macroinvertebrates (Barbour and snow/ice cover on both landscape and wider geo-
graphical scales. It also embraces changes in UVB Changing Chemical Environment

exposure associated with ozone depletion and Invertebrates have been suggested as bioindicators
more localized and obscure effects such as changes of a range of chemical changes occurring in aquatic
in soil properties associated with compaction by and terrestrial environments. These can involve a sin-
skiing (Kopeszki and Trockner 1994). By contrast with gle chemical parameter such as pH, the concentration
terrestrial ecosystems, the effects of the primary physi- of a single heavy metal pollutant such as cadmium, or
cal parameters, especially current, substrate type, excess amounts of plant nutrients, especially nitrogen
depth, and temperature, on invertebrates are much and phosphorus (Brodersen and Andersen 2002). A
more widely understood in aquatic ecosystems (Allan direct relationship can be established between the
1995). concentration of the chemical and the performance of
Several authors have suggested that invertebrates one or more indicator species. For example, the mayfly
can serve as useful bioindicators of current and past Hexagenia has served as a sentinel organism in the
temperature changes (e.g., Parsons 1991, Kopeszki and Great Lakes and large rivers of North America, indi-
Trockner 1994, Danks 1992, Brodersen and Anderson cating when eutrophication resulted in lethal anoxic
2002, Coope and Lehmdahl 1996, Hogg and Williams conditions beginning in the 1950s, and the rebirth of
1996, Hodkinson and others 1999, Hodkinson and these ecosystems (Fremling 1991, Krieger and others
Bird 1998, Bird and Hodkinson 1999, Bale and others 1996). Hexagenia tusks in the lake beds provide a view
2002) in both terrestrial and aquatic environments. of human impacts looking back over the last 300 years
The confirmatory criteria are generally changes in (Renoldson and Hamilton 1993). More frequently,
species distribution and abundance over medium to however, chemical changes may involve a cocktail of
long time scales. More recently, measurements of FA chemical effects that combine several compounds
have shown increased levels of developmental asym- simultaneously. Here it becomes exceedingly difficult
metry resulting most probably from thermal stresses to unravel the independent effects of each compound
experienced by aquatic invertebrates over shorter on the individual species, and often the invertebrate
developmental time scales. This suggests that sublethal community or some subset thereof is used to indicate
traits such as FA within populations of selected species some general measure of ecosystem ‘‘health’’ or level
may prove useful, indicating more subtle changes in of pollution such as ‘‘water quality.’’ Much work also
the thermal environment (Savage and Hogarth 1999, remains to be done on the synergistic effects of
Hogg and others 2001, Mpho and others 2002). The chemicals and the manner in which this affects inver-
general significance of FA in biomonitoring is dis- tebrate responses (Belden and Lydy 2001). Clements
cussed separately later. and others (2002) recently demonstrated how a com-
Invertebrates may also prove useful in indicating bination of descriptive and experimental approaches
factors linked to precipitation, such as soil moisture. help to focus arguments when faced with multiple
Several species of Collembola, oligochaete worms, and causal factors. Table 1 gives a selective list of examples
Diptera larvae show declining abundance with reduced where chemical changes occurring in aquatic and ter-
soil moisture (Convey and others 2003, Briones and restrial ecosystems have been suggested as systems that
others 1997). can be monitored using invertebrate bioindicators.
Many, but not all, invertebrates appear directly Sublethal effects of stress associated with several forms
sensitive to varying levels of UV radiation (e.g., Kiffney of pollution have also been documented, showing
and others 1997, Kelley and others 2003, Tank and changes in the levels of FA in several species of aquatic
others 2003). The direct effects of exposure, for and terrestrial invertebrate (see later).
example, among zooplankton, are well documented
and include behavioral modification and increased
mortality levels, dependent on species (e.g., Hader and Habitat Quality and Conservation Value
others 1998). More subtle responses, with bioindica- At the simplest level, a basic inventory of the eco-
tion potential, occur among leaf beetles (Chrysomeli- logically important species that might be affected by a
dae) that exist as different polymorphic forms with planned development may be considered when draw-
different reflectivity of UV radiation (Mikhailov 2001). ing up a statutory Environmental Impact Assessment
In several species, the proportion of UV-tolerant forms for a given site. The bioindicator may be merely the
increases with altitude and parallels the trend in inci- number of rare, local, or endangered species (Rosen-
dent radiation. This corresponds with the relationship berg and others 1986). However, one of the main basic
between pigment color in zooplankton and UV expo- problems of conservation biology is to establish the
sure (Tartarotti and others 2001). relative value and importance of the ecological com-
Table 1. Selected recent and specific examples to illustrate the range of chemical factors in aquatic and
terrestrial environments that have potential for being biomonitored by invertebrates
Chemical/pollutant Invertebrate group Reference
Aquatic
pH/acidification General lotic invertebrates Clenaghan and others 1998, Larsen
and others 1996
Lentic invertebrates Lonergan and Rasmussen 1996
Lentic chironomids Mousavi 2002
Nitrogen and phosphorus Lotic insects with pathogenic Lemly 2000, Lemly and King 2000
microorganisms
Lentic chironomids Brodersen and Lindegaard 1997
Heavy metals Lentic Chaoborus Croteau and others 2002
Lotic nematodes and ciliates Fenske and Gunther 2001
Benthic invertebrates Grumiaux and others 2000, Nelson 2000,
Cain and others 1992
Caddisflies Aizawa and others 1994
Organic toxicants Lotic nematodes and ciliates Fenske and Gunther 2001
Cladocera Baldwin and others 2001, Guilhermino
and others 2000
Benthic invertebrates Grumiaux and others 2000
Pesticides Benthie invertebrates Fulton and Key 2001
Lentic zooplankton Kreutzweiser and Faber 1999
Dragonflies Takamura and others 1991
Coal mine runoff Trichoptera Fernandez-Alaez and others 2002
Terrestrial
pH/acidification Soil microarthropods van Straalen 1998
Heavy/trace metals Several soil invertebrates Cortet and others 1999, van Straalen 1998,
Dallinger 1994
Sarcophagid flies Bartosova and others 1997
Air pollution/ acid deposition Several invertebrates Saldiva and Bohm 1998
Spiders Horvath and others 2001
Collembola Kopeszki 1997, Steiner 1995
Cryptostigmatic mites Sterner 1995
Day flying Lepidoptera Kozlov and others 1996
Nitrogen inputs Collembola Kopeszki 1997
Pesticides Collembola Frampton 1997
Soil microarthropods Trublayevich and Semenova 1994
Various soil invertebrates Cortet and others 1999
Asbestos Sarcophagid flies Bartosova and others 1997
munities inhabiting a range of habitats. This is often a previously. Generally, evaluation will be made on the
precursor to the selection of unique or representative basis of a single set of samples and will not necessarily
areas to achieve stated conservation strategy objectives. involve repeated measurement over time (monitor-
Areas may vary in size from small local reserves to major ing).
fragments of habitat such as regional forests (Statzner Table 2 illustrates the diversity of invertebrate taxa
and others 2001). Furthermore, additional factors that have been suggested as good bioindicators of
including habitat seasonality (Euliss 2002) and ecotone habitat quality. Most of them are relatively untested,
effects (Boscaini and others 2000) may complicate the and formal protocols for their use as indicators are not
issue. in place. They often represent the work of a single
Clearly it is impractical to collect full comparative specialist, and although the results describe meaning-
inventories of every species present in all areas, and a ful trends within the chosen taxon, it is often not always
measure of subsampling using selected taxa is re- clear how reflective the results are of the whole com-
quired. Subsampling needs to reflect as accurately as munity and whether the taxon represents the best
possible the trends that would be likely to occur in a biodiversity indicator for that particular community. It
full data set, taking into account the important criteria may be that favored invertebrate groups, such as but-
for community subset sampling and evaluation listed terflies, are given higher subjective weighting than
Table 2. Selected recent examples of the suggested use of indicator invertebrates for evaluating habitats for
biodiversity, condition, and structure
Habitat Invertebrate group Reference
Terrestrial
General (habitat continuity) Fungivorous beetles Sverdrup-Thygeson 2001
General (quality) Spiders Riecken 1999, Paoletti and Hassall 1999
Diptera Frouz 1999
Coccinellid beetles Iperti 1999
Syrphid flies Haslett 1997b, Sommaggio 1999
Staphylinid beetles Bohac 1999
Cryptostigmatic mites Behan-Pelletier 1999
Rare beetles Franc 1994
Tiger beetles Pearson and Cassola 1992
Butterflies Brown and Freitas 2000
Landscape and habitat features Lepidoptera, spiders, carabid beetles Jeanneret and others 2003
Agroecosystems Heteropterous bugs Fauvel 1999
Ants Peck and others 1998
General invertebrates Buchs and others 2003
Savanna grassland Dung beetles McGeoch and others 2002
Grassland Collembola Greenslade 1997
Forest Fungivorous insects Jonsell and Nordlander 2002
Boreal forest Coleoptera Jonsson and Jonsell 1999
Rangeland Ants Andersen and others 2004
Aquatic
Aquatic ecosystems (general) Interstitial invertebrates Claret and others 1999
General invertebrates Charvet and others 1998
River (typology) Lotic invertebrates Cayrou and others 2000
Stream (habitat integrity) Benthic invertebrates Buffagni and Comin 2000
Stream (morphological integrity) Benthic invertebrates Jansen and others 2000
Lakes Chironomid midges Brodersen and Lindegaard 1999
Ponds Odonata and Trichoptera Briers and Biggs 2003
Streams Plecoptera Helesic 2001
Headwater streams Macron vertebrates Heino and others 2003a
Rivers Benthic invertebrates Lang 2000
Seasonal and temporary wetlands Aquatic invertebrates Euliss and others 2002
Freshwater littoral Macroinvertebrates White and Irvine 2003
their less aesthetically attractive community consorts that this entails. There is clearly a trade-off between the
such as, for example, the ants. The latter may be, for number of taxa that can be ‘‘captured,’’ the taxonomic
example, less well studied but better indicators of level at which one operates, and the land area needed
comparative biodiversity. Furthermore, where the same to conserve biodiversity as defined by the criteria used.
habitat units have been assessed using different subsets The application of the concept of complementarity
of invertebrate taxa, there is often surprisingly little defined by Reyers and others (2000) offers one way in
commonality in the results obtained (McGeoch 1998, which the assessment of biodiversity can be optimized
Reyers and others 2000), although in others the level when choosing reserve areas.
of congruence may be high (Saetersdal and others A further suggested use of invertebrates is in the
2003). assessment of habitat continuity in which the presence
Another major problem is taxonomic comparability of certain species is used to bioindicate long-term sta-
among samples from spatially dispersed areas. The bility or unchangeability within the habitat over time
more samples taken from a wider area, the more likely (Norden and Appelqvist 2001). Indicator taxa such as
it is that the level of taxon overlap, particularly at the land snails and certain fungus-feeding beetles associ-
species level, will decline. This raises the question of ated with persistent forest fungi have been suggested as
whether it is more appropriate to work at the species indicating such long-term stability within woodland
level or whether it is better to work at a higher taxon (Norden and Appelqvist 2001, Sverdrup-Thygeson
level, with all the loss of species-specific information 2001).
Table 3. Selected recent examples of the suggested use of invertebrates as indicators of habitat management,
degradation, restoration, and improvement
Change indicated Invertebrate group Reference
Grassland topsoil removal Carabid beetles Sieren and Fischer 2002
Land management practice Ants Andersen and others 2002
Dispersing insects Mora and others 2004
Extent of logging Spiders Willett 2001
Dung beetles Davis and others 2001
Stream macroinvertebrates Bojsen and Jacobsen, 2003
Mining disturbance in savanna Grasshoppers Andersen and others 2001
General ecosystem health Many invertebrates Hilty and Merenlender 2000
Landscape/ecosystem sustainability Many invertebrates Paoletti 1999b
Soil invertebrates Duelli and others 1999
Earthworms Paoletti 1999a
Impact of genetically modified crops Invertebrates Haughton and others 2003
Soil management Soil invertebrates Enami and others 1999
Change in general habitat quality Bees and wasps Tscharntke and 1998
Forest restoration General invertebrate community Jansen 1997
Farming impacts Protozoa Foissner 1997
Forest degradation Tiger beetles Rodriguez and others 1998
Various insects and nematodes Lawton and others 1998
Sheep grazing Several insect groups Gibson and others 1992
Grassland management Coleoptera and Orthoptera Jonas and others 2002
Pollutant effects on forest Scolytid beetles Grodzki 1997
Forest disturbance Butterflies Hamer and others 1997
Moths (Arctiidae and Notodontidae) Summerville and others 2004
Forest management Mycetophilid flies Okland 1994
Forest floor invertebrates Schowalter and others 2003
Longicorn beetles Maeto and others 2002
Grassland habitat disturbance Hemiptera Auchenorrhyncha Nickel and Hildebrandt 2003
Urbanization Carabid beetles Sustek 1992
Habitat fragmentation Ants, Coleoptera, Arenaea, Diptera, other Hymenoptera Gibb and Hochuli 2002
Water quality/habitat integrity Benthic invertebrates Kashian and Burton 2000
Stream restoration Bethic invertebrates Muotka and others 2002
Habitat Change, Degradation, and Recovery others and, when used sensibly as part of a monitoring
Ecological change, through the process of succes- program over time, can mirror and thereby bioindicate
sion and species change (community assembly in the processes of change. As in the case of biodiversity
modern parlance), is a natural trend that occurs over assessment, there are many suggested indicator taxa of
time after the creation of new habitat. It may also take habitat change, but again their comparative suitability
place after catastrophic loss of soil and vegetation cover often remains untested (Table 3). A suitable single
through natural disturbance. Many habitats, however, biomonitor species will respond sensitively to the
have been subjected, through a variety of agencies, to changes taking place but will have sufficient resilience
nonnatural alteration. These agencies of change often not to go extinct, that is, broad tolerance. It is, how-
involve negative human impacts such as land use ever, the changing species balance within a wider
modification, pollutant input, agricultural practices, community that often serves better to indicate change.
etc., often leading to habitat degradation and reduced The well-tried example of organic pollution effects in
biodiversity. Relaxation of these imposed stresses, par- lotic ecosystems again illustrates this principle well. As
ticularly when accompanied by active restoration pro- pollution gradually increases, the invertebrate commu-
grams, leads to habitat recovery and improved nity shifts from one dominated by stoneflies, mayflies,
biodiversity. Biomonitoring may also include forward- and caddisflies to one in which chironomid midges and
looking assessments aimed at predicting landscape or tubificid worms predominate. Remove the stress and the
ecosystem sustainability (Paoletti 1999b). Some inver- previous community balance is restored. Similar species
tebrate taxa are more sensitive to these changes than replacement takes place during succession.
Which Organisms and Measures are the Most Selection of Bioindicator Organisms
Useful and Why? Before choosing a suitable bioindicator system, it is
first necessary to define clearly the objectives and
The advantages of including biological monitoring
endpoints of the study (McGeoch 1998). This should
and evaluation systems over those that rely only on
include a statement of exactly what it is intended to
physical and/or chemical data have already been
measure, how it will be measured, and why. It needs to
clearly stated (Hellawell 1986, Rosenberg and Resh
take into account the nature of the problem, whether it
1993). Put succinctly, living organisms occupy their
is a response to a single pollutant at a restricted site or
habitat continuously and experience the stresses,
an attempt to compare biodiversity over a broader area.
changes, or modifications taking place therein. Their
The spatial and temporal scales over which the study is
response integrates the cumulative effects of environ-
conducted require special consideration. Lack of pre-
mental change over time, and they may be sensitive to
cision at this stage will result in inappropriate bioin-
several different stresses simultaneously. This includes
dicators being chosen and results that are difficult to
pulsed inputs of pollutants or pulsed disturbances that
interpret. Only after the groundwork has been estab-
may not be picked up by spot chemical monitoring,
lished can a suitable indicator system be selected to
although again the impact of pulsed disturbance may
support the strict protocols necessary. Sometimes taxa
vary among communities (Collier and Quinn 2003).
that are good bioindicators on one spatial scale may
Biological organisms are, nevertheless, good long-term
lose their reliability at higher or lower scales, raising
indicators of ecosystem health, and biological moni-
questions about how stable their measured response is
toring allows us to focus, at least initially, on environ-
(Allen and others 1999). Similarly, different groups of
mental changes that elicit significant biological
organisms display contrasting responses on temporal
responses. Having established that organisms serve a
scales. Response times in microorganisms can be a
useful function as biomonitors, how do we decide
matter of hours; those in trees and larger vertebrates
which are the best groups of organisms to use?
are measured in years. Clearly, the best bioindicators
Why Use Invertebrates? show consistent responses over a wide range of spatial
and temporal scales.
Invertebrates are abundant medium-sized organ-
The criteria for the selection of bioindicator
isms that, as a generality, have growth rates and pop-
organisms were detailed by Hellawell (1986), Pearson
ulation turnover times lying midway between those of
(1994), McGeoch (1998), Cortet and others (1999),
microorganisms and higher plants and animals. Inver-
and Hilty and Merenlender (2000). The appropriate-
tebrates also have effective active and passive dispersal
ness of particular criteria depends on the nature and
mechanisms that often allow wide dissemination and
scale of the problem addressed.
rapid recolonization of disturbed habitats (Hodkinson
The prime generic criteria are as follows:
and others 2002). Because of their slow population
turnover times and slower dispersal, plants are rela-
1. Higher and/or lower taxa chosen have well-known
tively less responsive indicators of change. At the
and stable taxonomy, with ease of identification
opposite extreme, microorganisms, with their very ra-
emphasized.
pid responses to changing environmental conditions,
2. Biology of organisms is well known, particularly in
tend to fluctuate more wildly and be less stable indi-
response to stress factors or to changes in habitat
cators of longer-term trends. Finally, there is evidence
properties of interest.
that invertebrate responses are also indicative of
3. Organisms are abundant, straightforwardly sur-
changes in ecosystem function (Wallace and others
veyed, and easily manipulated.
1996). Having thus established that invertebrates
4. Higher and lower taxa chosen are distributed on a
probably have the better overall potential to serve as
scale that matches the spatial and temporal
good bioindicators, the problem then is choosing
requirements of the study.
which organisms or subsets of communities to use. As
5. The chosen taxon or groups of taxa are represen-
has already been shown, a multitude of different
tative of the whole community, or, if not, then their
aquatic and terrestrial invertebrates from protozoa,
responses are strongly correlated with a known
oligochaete and nematode worms, isopods, micro-
stress factor.
crustacea, Collembola, mites, spiders, and insects have
all been suggested as bioindicators. Which of them,
however, is the best or most appropriate for a partic- In addition, a number of other issues should be
ular situation remains a question for debate. considered. These include the economic significance
or aesthetic appeal of the biomonitoring group chosen measure(s) remains controversial and subject to in-
and the logistics and cost of biomonitoring and eval- tense analysis. For example, there have been numerous
uation compared with alternative methodologies. The articles written on the strengths and weakness of mul-
ideal system is inexpensive, simple, easy to implement, timetric and multivariate measures of invertebrate re-
quick, reliable, and easily understood by nonprofes- sponses in streams (Gerritsen 1995, Norris 1995,
sionals. This ideal clearly is hardly ever achievable, and Renoldson and others 1997). Similarly, FA has been
any biomonitoring system is a compromise between criticized, and attempts have thus been made to de-
precision and cost. There is, nevertheless, an inherent velop a more refined and robust methodology (Leung
danger that chosen indicator systems can become and Forbes 1997, Leung and others 2000, Bjorksten
overcomplicated relative to the problems being ad- and others 2000, Lens and others 2002). In the end,
dressed. It is important, therefore, that the methodol- each approach has strengths and weaknesses. The
ogy be optimized for the parameters being used challenge is to incorporate this information in the
(Rabeni and Wang 2001, Bailey and others 2001). process of developing and modifying monitoring pro-
tocols.
Taxonomic Challenges
One of the main problems in using invertebrates as Specific Use of Bioindicators in Mountain
bioindicators is the sheer number and range of species
Areas
that potentially could be used. This inevitably leads to
problems of species identification. Taxa differ mark- Mountain landscapes represent steep gradients for a
edly in the ease with which they can be identified by wide range of environmental parameters, particularly
nonspecialists, and some of the taxa suggested for bi- temperature, precipitation, UV radiation, atmospheric
omonitoring can only be reliably identified by taxo- gas concentrations, and so on. This is reflected in the
nomic specialists. Thus, a group of invertebrates may adaptations and distributions of varying types of
be shown to be excellent indicators, but their wide- organisms and ecological communities that occupy
spread and regular use could be precluded by taxo- different positions along these gradients, both in ter-
nomic difficulties. One way around this problem is to restrial and aquatic ecosystems. Many of the environ-
analyze quantitatively the levels of predictability mental factors that affect the organisms are
achieved using successively higher levels of taxonomic multifaceted and interlinked. For example, precipita-
resolution (Rabeni and Wang 2001, Bailey and others tion can fall as rain or snow. The rain can run off to
2001). It may be, for example, that genera have the form streams and river ecosystems; the snow may re-
same predictive power as species. If this is the case, main, either seasonally or permanently, creating un-
then it is unnecessary to identify the animals down to ique snowbed environments. Precipitation interacts
species (Lenat and Resh 2001). For aquatic inverte- with temperature through snow insulation effects and
brates, professional and volunteer monitoring pro- thermal buffering of environmental temperatures
grams often rely on higher taxa, whereas others rely on within moist terrestrial and aquatic habitats. The harsh
species-based protocols (e.g., Carter and Resh 2002, environmental conditions combined with the isolated
Engel and Voshell 2002). A confounding factor in and fragmented nature of many alpine areas means
resolving this controversy may be the limited informa- that they serve as a focal point for microevolution and
tion that is available for the vast majority of aquatic and adaptation in particular groups of organisms (Haslett
terrestrial species. For example, quantitative observa- 1997a) and contribute to their unique biodiversity. The
tions of responses to complex environmental stresses combination of relatively specialized species and nat-
are rarely available, and the general applicability of urally harsh conditions makes animal communities at
observations is often unknown because levels of genetic high altitude especially vulnerable to environmental
variation within and among populations are unclear, disturbance, particularly anthropogenic pollution and
and the plasticity of responses to environmental stress changing climate. This vulnerability often gives alpine
is largely untested. Even so, invertebrates clearly offer areas high conservation significance. Alpine environ-
an important source of information concerning envi- ments and their invertebrate communities are gener-
ronmental conditions. ally subject to less direct pollution and disturbance
relative to many of the surrounding low-elevation areas
Measures of Invertebrate Responses because agricultural, industrial, and residential devel-
As indicated above, invertebrates can be used to opment is far less intense. However, environmental
assess environmental stress using a variety of individual, degradation from anthropogenic activities is still com-
population, and community measures. The choice of mon in alpine areas. For example, they have been
subjected to intensive land use, including forest harvest as noted earlier (Whittaker and Tribe 1996), exhibit
and management, livestock and dairy production, rapid, often year-to-year variation in their upper alti-
mining, and most recently, recreation, for hundreds, if tudinal limit in response to changing mean temper-
not thousands of years. In addition, aerial dispersion atures.
and deposition results in significant exposure to a wide Often the relative time scales of change can be
range of gaseous and/or particulate pollutants. In- important. Herbivorous invertebrate species frequently
creased deposition of nitrogen, for example, tends to respond more sensitively to changing temperatures
occur in areas of high precipitation (Morecroft and over shorter time scales than their host plant. For
Woodward 1996). example, the three congeneric species of jumping
Invertebrate communities are distributed along plant louse living on fireweed (Chamerion angustifolium)
these steep altitudinal gradients in relation to their in North America each have characteristic altitudinal
particular environmental tolerances and respond distributions within the much broader altitudinal dis-
accordingly when environment conditions change. tribution of their host and might be expected to re-
However, despite their clear potential, there are few spond to rising temperatures in different ways. The
well-established invertebrate biomonitoring systems high-altitude species, Craspedolepta schwarzi, might van-
that are commonly and widely used to monitor change ish as suitable alpine habitats disappear. The two lower-
in montane environments, especially among terrestrial altitude species, C. nebulosa and C. subpunctata, might
invertebrates. be expected to exhibit an upwards extension of their
Mountain communities may potentially respond to overlapping ranges, but with C. nebulosa always occu-
disturbance in different ways. For example, species pying a slightly higher elevation than C. subpunctata
richness and diversity will most probably decrease in (Hodkinson and Bird 1998, Bird and Hodkinson
response to many types of chemical pollution. By 1999). Similar altitudinal changes in species distribu-
contrast, warming, additional precipitation, or in- tions in response to temperature are likely to occur
creased nutrient loading within limits is likely to pro- among invertebrates occupying mountain streams
duce overall increases in species richness and diversity. where temperature also affects dissolved oxygen avail-
This may, however, be accompanied by the loss of true ability (Devan and Mucina 1986, Jacobsen and others
alpine species as the environment becomes more be- 2003). Although these examples illustrate the potential
nign and species immigration and establishment from of mountain dwelling invertebrates as bioindicators,
lower elevations takes place. True alpine species can- rigorous and fully tested protocols with wide applica-
not shift their ranges upwards above the tops of bility remain to be developed.
mountains. There also may be a temporal component
that needs to be considered in assessing a response. For
example, an alpine site may experience a rapid drop in
Acknowledgments
species richness as temperature thresholds are ex-
The paper was conceived at an international work-
ceeded, but then experience a long-term gain in spe-
shop organized by Rüdiger Kaufmann and Leopold
cies richness as soils and vegetation change and
Füreder (Institute of Zoology and Limnology, Univer-
mature, and as immigration brings new invertebrate
sity of Innsbruck) to review critically the use of inver-
species to the site. The research challenge is to identify
tebrates for monitoring long-term impacts of
the range of expected responses to defined impacts.
environmental change in mountain habitats. We thank
Nevertheless, selected invertebrates, if used judi-
the Austrian Academy of Sciences for providing the
ciously as outlined previously, can act as good in situ
opportunity and financial support that made our
biomonitors for a wide range of environmental fac-
deliberations possible. JKJ was also supported by Na-
tors that impinge upon mountain ecosystems. They
tional Science Foundation Grant DEB-0424681, the
have high potential for monitoring physical and
Pennswood Endowment Fund, and the Stroud Water
chemical changes within the environment, they can
Research Center Endowment Funds.
bioindicate differences in the patterns of biodiversity
across the landscape, and they can be expected to
respond to deteriorating or improving habitat quality
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Terrestrial and Aquatic Invertebrates as Bioindicators

graphical scales. It also embraces changes in UVB Changing Chemical Environment

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