How Is Ecosystem Health Defined and Measured? a Critical Review of Freshwater and Estuarine Studies

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Ecological Indicators 69 (2016) 722–729

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Ecological Indicators

jo urnal homepage: www.elsevier.com/locate/ecolind

Review

How is ecosystem health deﬁned and measured? A critical review of

freshwater and estuarine studies

∗

Allyson O’Brien , Kallie Townsend, Robin Hale, David Sharley, Vincent Pettigrove

Centre for Aquatic Pollution Identiﬁcation and Management (CAPIM), School of Biosciences, University of Melbourne, Victoria, 3010, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Assessing ecosystem health is an ongoing priority for governments, scientists and managers worldwide.

Received 15 January 2016

There are several decades of scientiﬁc literature discussing ecosystem health and approaches to assess

Received in revised form 22 April 2016

it, with applications to aquatic and terrestrial environments incorporating economic, environmental and

Accepted 2 May 2016

social processes. We conducted a systematic review of studies that assess ecosystem health to update our

Available online 2 June 2016

current understanding of how ecosystem health is being deﬁned, and provide new ideas and directions

on how it can be measured. We focused the review on studies that used the term ‘ecosystem health’ or the

Keywords:

equivalent terms ‘ecosystem integrity’, ‘ecosystem quality’ and ‘ecosystem protection’, in lotic freshwa-

Ecosystem integrity

Freshwater ter and estuarine environments, and examined how many of these included explicit deﬁnitions of what

Estuarine ecosystem health means for their study system. We collected information about the temporal and geo-

Community graphical distribution of studies, and the types of indicators (biological, physical or chemical) used in the

Ecology assessments. We found few studies clearly deﬁned ecosystem health and justiﬁed the choice of indica-

Management tors. Given the broad use of the term it seems impractical to have an overarching deﬁnition of ecosystem

health, but rather an approach that is able to deﬁne and measure health on a case by case basis. A combi-

nation of biological, physical and chemical indicators was commonly used to assess ecosystem health in

both estuarine and freshwater studies, with a strong bias towards ﬁsh and macroinvertebrate community

metrics (e.g. diversity, abundance and composition). We found only two studies that simultaneously con-

sidered both freshwater and estuarine sections of the ecosystem, highlighting the signiﬁcant knowledge

gap in our understanding of the transfer of ﬂow, nutrients and biota between the different systems—all

key factors that inﬂuence ecosystem health. This review is the ﬁrst to combine knowledge from both

freshwater and estuarine ecosystem assessments and critically review how aquatic ecosystem health is

deﬁned and measured since the late-1990s, providing the basis for setting achievable management goals

relating to ecosystem health into the future.

Contents

1. Introduction ...... 723

2. Methods ...... 723

3. Results & discussion ...... 724

3.1. Deﬁning ecosystem health...... 724

3.2. Temporal and spatial distribution of studies ...... 725

3.3. Indicators used to assess ecosystem health ...... 726

4. Conclusions ...... 728

Acknowledgement ...... 728

References ...... 728

∗

Corresponding author.

E-mail address: [email protected] (A. O’Brien).

http://dx.doi.org/10.1016/j.ecolind.2016.05.004

A. O’Brien et al. / Ecological Indicators 69 (2016) 722–729 723

1. Introduction measures of ecosystem function with multi-metric indices and

other indicators of ecosystem structure may provide a better rep-

‘Ecosystem health’ is a common term used in environmen- resentation of whole ecosystem health (Woodward et al., 2012).

tal science and management as a way to describe the state of a Further progress in the way ecosystem assessments are approached

system relative to a desired management target or reference con- may continue to arise as molecular techniques, such as next-

dition (Rapport, 1989 Schaeffer et al., 1988). Other deﬁnitions of generation sequencing, become more cost-effective and new types

ecosystem health have emphasized the integration of ecological, of biodiversity indicators are developed (Forbes and Richardson,

economic and human processes (Rapport et al., 1998) and meas- 1913; Zinger et al., 2014).

ures of sustainability and system resilience (Costanza et al., 1992). Considering the broad use of the term ‘ecosystem health’ and

Ecosystem health can be linked to management and political objec- the many different deﬁnitions and assessment approaches, it seems

tives (Fairweather, 1999) and used in the context of environmental unrealistic to have an overarching deﬁnition of ecosystem health

management legislation and policies (Karr, 1990; Negus et al., (Costanza et al., 1992), but one deﬁned relative to the system

2009), as well as deﬁning different societal, recreational or com- being studied (Dobbie and Negus, 2013). Palmer et al. (2005)

mercial beneﬁts (Karr, 1999). Although ecosystem health is not a highlight that endpoints to stream restoration are unlikely to be

new term, but one that has been discussed and deﬁned in the lit- universally applied, and suggest that a ‘guiding image’ must be

erature since the late 1980s, achieving a state or condition that articulated to describe the most dynamic, ecologically dynamic

reﬂects a healthy ecosystem is an ongoing priority for government, state possible at a site, taking into account the likely inﬂuence of

scientists and managers worldwide (Burger et al., 2006). irreversible anthropogenic changes, such as alterations to catch-

Assessing ecosystem health can be approached in several dif- ment hydrology and geomorphology, the installation of permanent

ferent ways (Rapport et al., 1998). It can involve the identiﬁcation infrastructure (e.g. on ﬂoodplains or along coasts), and the spread

of certain characteristics that indicate a healthy ecosystem, such as of invasive species that cannot be easily removed. In a similar vein,

a river system that is free from algal blooms, has a high biological a range of information could be used to help determine what should

diversity or a particular biotic score (Di Battista et al., 2016; Pont reﬂect a ‘healthy ecosystem’, including historical information (e.g.

et al., 2006). Alternatively, the health of an ecosystem can be char- photographs, maps, survey records), appropriate reference sites,

acterized by ecosystem services that humans depend on, such as analytical/process based models, stream classiﬁcations, or in some

the provision of clean drinking water (Keeler et al., 2012), nutrient instances common sense (Palmer et al., 2005).

recycling and maintenance of biodiversity (US National Research Here, we present the results of a systematic review undertaken

Council, 2005). Ecosystem health assessments may also involve to update our current understanding of how ecosystem health is

predictions about food web functioning and different trophic lev- deﬁned and measured in lotic freshwater and estuarine environ-

els required to sustain a healthy ecosystem (Thompson et al., 2012), ments. Our ﬁrst aim was to identify studies seeking to measure

or an ecosystem’s ability to maintain structure and function when ecosystem health, and then to examine how many of these included

confronted with external stress (Mageau et al., 1995). an explicit deﬁnition of what ecosystem health means for their

In aquatic ecosystems, there is now more pressure than ever for study system. Our second aim was to examine the spatial and

appropriate monitoring and management strategies that will main- temporal distribution of studies that had the primary goal of mea-

tain ecosystem health. With over 50% of the world’s population suring ecosystem health or equivalent (i.e. ecosystem integrity,

living within three kilometers of freshwater (Kummu et al., 2012) quality or protection) in lotic ecosystems (i.e. freshwater, streams,

and many of the largest cities around the globe situated on estuaries rivers, waterway or estuaries), to examine if they are geograph-

(Boesch, 2000; Johnston et al., 2015b), these ecosystems are con- ically biased and whether these types of studies are becoming

tinually under pressure from an array of anthropogenic stressors increasingly common through time. Geographic biases can hinder

(Halpern et al., 2008; Vorosmarty et al., 2010). Contamination, habi- conservation efforts, for example, if the location of research is mis-

tat degradation and non-indigenous species are among the main aligned with research needs or priorities (Lawler et al., 2006). Our

threats that affect aquatic ecosystem health through changes in third aim was to examine how ecosystem health is being assessed,

community composition and biological diversity, ecological func- in terms of the types of indicators that are being used (i.e. chemical,

tioning and provisioning of ecosystem services (Tolkkinen et al., biological, physical), and for biological indicators, the level of orga-

2016). nization at which they are monitored (i.e. individual, population,

Assessing aquatic ecosystem health has been an ongoing theme community), and the taxonomic groups that are commonly stud-

in the scientiﬁc literature for several decades, possibly originating ied. We use the results of our study to critically evaluate ecosystem

with river health indicators such as the Index of Biotic Integrity health assessments in lotic freshwater and estuarine environments,

(Karr, 1981, 1991) or even earlier with the development of the identify key knowledge gaps, and ultimately aid in the development

Saprobic Index to assess water quality (Friedrich et al., 1992; of robust and appropriate approaches to assess ecosystem health

Kolkwitz and Marsson, 1909) and biological surveys of whole river in the future.

(Forbes and Richardson, 1913) and lake ecosystems (Thienemann,

1925). There are now many approaches for assessing the health

of freshwater and estuarine systems that use biological commu- 2. Methods

nity measures either separately or in combination with chemical

or physical parameters. Multi-metric indices are useful in that The systematic review followed the method of Pickering and

they can distill a lot of information and parameters onto a uni- Byrne (2014). We reviewed studies that assessed ecosystem health

form scale that can be easily used to make management decisions. in lotic freshwater and estuarine environments (rivers, streams and

However, they are not always transferrable between regions or estuaries) which excluded marine, wetland, lake and lagoon sys-

countries, often depend on comparisons with appropriate refer- tems to keep the scope of the study manageable. Search terms

ence conditions and rarely provide information on what aspects of were “ecosystem health” and similar phrases that are often used

the ecosystem are responsible for changes in health (Borja et al., interchangeably; “ecosystem integrity”, “ecosystem quality” and

2012; Pont et al., 2006). Measures of ecosystem function, such “ecosystem protection” plus freshwater or river* or stream* or

as respiration, primary productivity, metabolism and decomposi- waterway or estuar*. These terms were used in a multi-database

tion, are becoming more common in ecosystem health assessments search using Web of Science Core Collection, CABI: CAB Abstracts

(e.g. Bunn and Davies, 2000; Woodward et al., 2012). Combining and Global Health, Current Contents Connect and SciELO Citation

724 A. O’Brien et al. / Ecological Indicators 69 (2016) 722–729

Index. There were no restrictions on the date range. We limited Biological measures were categorized according to levels of

the search to peer-reviewed journal articles that could be accessed biological organization: individual, population or community.

through the online database to minimize any bias created by author Individual measures included morphology, pathology, behavior,

background knowledge and search patterns. Many bioassessment bioaccumulation/bio-concentration, survival, histological, molec-

and biomonitoring studies have the purpose of assessing ecosys- ular, larval settlement, growth and reproduction. Population

tem health (or quality, integrity or protection) and these studies measures included abundance, reproductive output/fecundity,

were captured in our literature search if they used these speciﬁc population growth and biomass. The majority of studies used

terms. However, we did not include the terms ‘bioassessment’ or community measures and so these were further categorized as

‘biomonitoring’ in the literature search so that our search remained measures of tolerance (e.g. Hilsenhoff, SIGNAL, Index of Biologi-

focused on the central theme of our study. cal Integrity), diversity (e.g. Shannon-Wiener, Simpson, Evenness),

It is possible studies that had the primary purpose of assessing abundance (total number of taxa, number of individuals, number

ecosystem health may have used the terms ‘river health’ or ‘stream of individuals in each taxonomic group), composition (% of each

integrity’ or ‘estuary health’ instead of ‘ecosystem health’ and so taxonomic group), biomass and traits (e.g. guild, functional group,

would not have been selected by our search. To understand the native/introduced) (Aazami et al., 2015), with an ‘other’ category

likelihood of this affecting our search we did a comparison between that included metrics that were less common (e.g. ﬁsh parasite

the number of records returned with what we think are other load, disease, catch per unit effort, stable isotope analysis). The

commonly used phrases: ‘river health’ versus ‘ecosystem health’, taxonomic groups for each biological measure were recorded as

‘waterway health’ versus ‘ecosystem health’, ‘estuary health’ versus bacteria, bioﬁlms, zooplankton, algae (including macroalgae and

‘ecosystem health’, ‘stream integrity’ versus ‘ecosystem integrity’. phytoplankton), plants, macroinvertebrates or ﬁsh.

In all cases, ‘ecosystem health’ or ‘ecosystem integrity’ returned

the most number of records, and when we compared a sub-set

of the records, around 20% were duplicated in both searches. We 3. Results & discussion

are conﬁdent that most studies that used different terms (i.e. river

health, stream integrity or estuary health) were also identiﬁed 3.1. Deﬁning ecosystem health

with our search terms. If there were studies that were missed

by our search because they used different terms, we think these We found less than 15% of studies that used the term ‘ecosystem

were minor omissions and did not affect the main outcomes of health’ or ‘ecosystem integrity’ or ‘ecosystem quality’ or ‘ecosystem

the review. A total of 2570 records were returned and imported protection’ had the primary aim of assessing it in lotic freshwa-

into a reference management tool (Endnote version X6.0.1). Dupli- ter and estuarine environments (n = 191 studies). Thirty-three of

cates were deleted leaving 1300 records to be searched manually. these studies were in estuaries, 156 were freshwater and two stud-

Our focus was on lotic freshwater and estuarine environments and ies in both the freshwater and estuarine sections of the ecosystem.

so we excluded studies that were conducted in lakes, wetlands, ‘Ecosystem health’ was the most commonly used term (127 studies)

lagoons, mangroves and marine habitats as well any study that with fewer studies using the equivalent ‘ecosystem integrity’ (42

was not a primary source of data (e.g. framework, management, studies), ‘ecosystem quality’ (18 studies) and ‘ecosystem protec-

index description, discussion papers and reviews). We recorded tion’ (4 studies). To reﬂect these results we use the term ‘ecosystem

the number of studies that speciﬁcally assessed ecosystem health health’ throughout this manuscript to encompass all of these sim-

and therefore used the term ‘ecosystem health’ or equivalent ilar search terms.

terms: ‘integrity’, ‘quality’ and ‘protection’. Studies that had indi- The majority of studies used ecosystem health as a general

rect statements, such as ‘these results could have consequences for descriptive term, often helping to put the study in a broader con-

ecosystem health’ were excluded. This information was typically text with potential management applications but without explicitly

in the ﬁnal paragraph of the introduction in each paper and so, assessing ecosystem health (n = 1109). These studies typically used

in most cases, to make this decision we accessed the paper. We single parameters, such as water quality, ﬂow or single species

also recorded the number of studies that deﬁned ecosystem health (e.g. Hasenbein et al., 2013) as an indicator of ecosystem health

or equivalent either within the introduction or method sections. and used indirect statements such as ‘the present investigation

The deﬁnition had to include speciﬁc predictions about how vari- suggests that contamination of aquatic ecosystems with oil could

ables, indicators or measures changed and/or related to ecosystem potentially affect ecosystem health. . .’ based on toxicity in a single

health. species (Ramadass et al., 2014), ‘detection of the protozoa in ﬁsh

Information recorded from each study included the study sys- may also be a good sentinel for environmental contamination or

tem (freshwater or estuary), the exact term used in the study ecosystem health’ (Reid et al., 2010) or ‘our recommendations will

(ecosystem health, integrity, quality or protection), type of study ensure ecosystem integrity’ (Aloo et al., 2013). Studies measuring

(experiment, survey or modelling) and measures used to assess the presence of contaminants were also common and often referred

ecosystem health (chemical, physical or biological). Chemical to those contaminants having potential consequences for ecosys-

measures used were further recorded as physico-chemistry (e.g. tem health (e.g. Aboul-Kassim and Williamson, 2003; Marentette

turbidity, dissolved oxygen, pH, electrical conductivity, and tem- et al., 2010). Only studies that speciﬁcally stated that they assessed

perature), nutrients, contaminants, (e.g. metals, pesticides and ecosystem health (n = 191) were considered further in this review.

hydrocarbons) or chlorophyll, with an ‘other’ category included for Deﬁning ecosystem health by having clear study objectives is

metrics that were less common (e.g. turbidity, E.coli and other faecal important to determine if management targets have been achieved

indicators). Physical measures were recorded as channel morphol- or whether actions should be adapted (Kolkwitz and Marsson,

ogy/dimension, ﬂow, substrate, land use or vegetation, with an 1909; Thienemann, 1925). This also requires an understanding

‘other’ category to record the less common metrics (e.g. redox of uncertainty or threshold limits that will trigger management

potential, altitude, annual runoff and sediment deposition). A ‘Pro- intervention if targets are not met (Friedrich et al., 1992). Only

cessing’ category included indicators that could not be categorized 28 studies had clearly deﬁned objectives and speciﬁc predictions

as physical or chemical, and were indicative of ecosystem function about parameters used to measure ecosystem health. Seven of

or ecological processes, such as measures of primary productiv- these studies were in estuaries and 21 were in freshwater envi-

ity, respiration, biochemical oxygen demand and decomposition ronments. These studies included clear predictions about how

rates. indicators used in the study were expected to change if the

A. O’Brien et al. / Ecological Indicators 69 (2016) 722–729 725

Fig. 1. Geographic and temporal distribution of studies that assess ecosystem health (or ‘integrity’, ‘quality’ or ‘protection’, all used in the literature search) in estuarine and

freshwater systems.

ecosystem was healthy, such as, low occurrence of larval defor- government policies, previously published literature or reﬂect the

mities (Diggins and Stewart, 1998), ecosystem health index score author’s personal interests (Lindenmayer and Likens, 2010) rather

greater than 85 (Davies et al., 2010), presence of planktonic large than statistical procedures and ecological importance. Irrespective

and juvenile stages of estuarine ﬁsh species (Ramos et al., 2012) or of the rationale, our review demonstrates the need for more care-

nitrogen concentrations below 2 mg N/L (Wiegand et al., 2010). ful planning and justiﬁcation of approaches for ecosystem health

There is no overall agreement on what it means to have a healthy assessments in both freshwater and estuarine environments.

ecosystem (Palmer and Febria, 2012), yet it is still necessary to have

clear deﬁnitions of ecosystem health on a study-by-study basis.

3.2. Temporal and spatial distribution of studies

For example, characteristics like low concentrations of contami-

nants and reduced biotic richness can indicate a severely degraded

The number of studies with the primary goal of assessing aquatic

ecosystem that is adjacent to protected forests, but may conversely

ecosystem health has increased over time (Fig. 1). We found only

indicate a reasonably healthy ecosystem in an urban environment.

freshwater studies (n = 21) prior to 2004, with 136 freshwater

In our review, we found an absence of clear study objectives and

studies, 33 estuarine and two in both environments since. The dom-

a lack of justiﬁcation about basic study design, including sampling

inance of freshwater studies prior to 2004 most likely reﬂects the

design, replication, choice of parameters and expected variability

inﬂuence of some key papers describing the concept of ecosystem

that either would or would not be acceptable depending on man-

health (Downes et al., 2002; Karr, 1999; Rapport, 1989) and the

agement targets. There is generally a bias in the literature towards

early development of the Index of Biotic Integrity for freshwater

the development of ecosystem health indicators (e.g. Chiu et al.,

ﬁshes (Karr, 1981). The number of ecosystem health publications

2011) and less discussion about the selection of reference sites (but

has steadily increased since the late 1990s and now includes estu-

see Borja et al., 2012), deﬁning levels of uncertainty and accept-

arine and freshwater, as well as marine environments (e.g. Barras

able limits (Dobbie and Clifford, 2015), meaningful effect sizes and

et al., 2014; Blomberg and Montagna, 2014). Although there are

sampling protocols that will detect ecologically relevant changes

journals dedicated to aquatic ecosystem health (Journal of Aquatic

(Dobbie and Negus, 2013). It is possible that decisions about what

Ecosystem Health, Ecosystem Health, and Aquatic Ecosystem Health

study design and parameters to use may be based on uncited

& Management) we found studies published across a wide range

726 A. O’Brien et al. / Ecological Indicators 69 (2016) 722–729

Fig. 2. Proportion of freshwater and estuarine studies that used (a) one, two or three indicators to measure ecosystem health, (b) physical indicators in the study, (c) chemical

indicators in the study, and (d) biological indicators at the individual, population or community level of organization.

of ecological, conservation and management journals (Supplemen- (Giling et al., 2015) as well as terrestrial and marine environments

tary Table S1 in the online version at DOI: 10.1016/j.ecolind.2016. (Conway-Cranos et al., 2015; Treasure et al., 2015) but, as our

05.004). Ecological Indicators had the most number of publications review highlights, there are still substantial knowledge gaps that

(n = 21) with over half of these studies published in the last three exist for freshwater-estuarine ecotones.

years (n = 11).

Based on geographic biases found by other reviews on conserva- 3.3. Indicators used to assess ecosystem health

tion (Lawler et al., 2006) and biodiversity research (Trimble and van

Aarde, 2012), we expected there may be more publications from the In any monitoring and assessment program, logistical con-

US and Europe with fewer studies from Asia, Africa and South Amer- straints (e.g. time, cost) are likely to mean that not all possible

ica. Instead, we found no strong bias in the distribution of studies variables can be monitored, and thus a subset of indicators must

between countries (Fig. 1). There were 35 countries represented be selected that relate to the goals of the project (Cairns et al.,

in this review and they all had around 80% freshwater and 20% 1993; Dale and Beyeler, 2001). In our review, most studies took the

estuarine studies. The exceptions to this were Korea, Canada and approach of using a combination of biological, physical and chem-

China, which all had signiﬁcant biases towards freshwater studies, ical indicators to assess ecosystem health, with over 80% of studies

while Portugal and the UK had mostly estuarine studies (Fig. 1). using two or three types of indicators (Fig. 2a). There were few stud-

Publications from China and Korea were particularly prevalent in ies that used only one type of indicator, although this was higher

the last three years (68% of studies from China and 62% of studies for estuarine studies (39%) compared to freshwater studies (15%)

from Korea were published in 2013–2015). The geographic distri- (Fig. 2a).

bution of ecosystem health assessments should ideally be focused The use of multiple indicator types in a study may provide a

in regions where this type of knowledge and research is most better assessment, but this needs to be accompanied by clear pre-

important, such as areas where impacts from human pressures are dictions about how they represent ecosystem health. Failing to

high and ecosystem health is most threatened (Trimble and van justify the selection of indicators is one of the main reasons moni-

Aarde, 2012). The increase in publications from China and Korea toring programs fail (Lindenmayer and Likens, 2010). Results from

most likely reﬂects the general increase in scientiﬁc output from this review have already shown that there are generally not a pri-

these countries (Veugelers, 2010), but may also be an indication ori deﬁnitions of ecosystem health (Palmer et al., 2005) and in

that new methods and approaches are being developed in these many cases there is no clear understanding of indicator responses

countries. Overall, these results indicate a positive shift towards to changes in ecosystem condition. Therefore, it is difﬁcult to deter-

addressing knowledge gaps and progressing our understanding of mine which combination of indicators is likely to reliably evaluate

what ecosystem health means for different ecosystems. the state of the ecosystem and success of the program.

Our review identiﬁed only two studies that assessed ecosys- The types of physical and chemical indicators used in ecosystem

tem health across both the freshwater and estuarine sections health assessments were mostly ﬂow and channel morphol-

of the ecosystem (Tolan and Nelson, 2009; Zhao et al., 2014). ogy/dimension (in freshwater studies only) (Fig. 2b) and nutrients

Understanding the transfer of water, nutrients, contaminants and and physico-chemistry (in freshwater and estuarine studies)

biota between the two systems is important for the develop- (Fig. 2c). Biota, more often than not, are used as indicators to

ment of appropriate indicators and approaches to monitoring reﬂect the condition of aquatic ecosystems (Vilmi et al., 2016).

ecosystem health. Cross-system subsidies of energy, nutrient and This was reﬂected in our results, with 82% of studies includ-

biota is reasonably well-understood for terrestrial and freshwater ing biological indicators at the community level of biological

A. O’Brien et al. / Ecological Indicators 69 (2016) 722–729 727

Fig. 3. Proportion of freshwater and estuarine studies that used (a) the different community metric and (b) taxonomic groups used in the ecosystem health assessments.

organization (Fig. 2d). Biological diversity, abundance, tolerance, taxa and ecosystem health are often assumed rather than demon-

and composition were all common community metrics used across strated, creating potential uncertainty about whether they are the

both freshwater and estuarine systems to assess ecosystem health most suitable indicators to be used. Our results highlight that there

(Fig. 3a). Community metrics has been successfully used for many are many parts of the biological community that are not being

years either as single or multi-metric indices to represent ecosys- measured, particularly microbiota (e.g. diatoms, microalgae, bacte-

tem health and inform management decisions (e.g. Chiu et al., ria, fungi). Microbiota could have different sensitives to human

2011). Community metrics are arguably the most ecologically rel- disturbance and could be equally as good or better as indicators

evant as they are more complete assessments of communities, of ecosystem health (Chen et al., 2016). It may be the case that

compared to individual or population metrics, and can be extrap- multiple taxonomic groups are routinely monitored to provide

olated to the state of an ecosystem through changes in species the most accurate assessment of ecosystem health (Vilmi et al.,

composition or food web structure (Attrill and Depledge, 1997). 2016). Rapidly developing new technologies and environmental

However, detecting change at the community-level can often be DNA monitoring tools (Rees et al., 2014) will enable more ﬂexi-

difﬁcult against highly variable background conditions (Gessner ble and cost-effective ways to sample biological communities, so

and Chauvet, 2002). This is when individual or population metrics we expect that microbiota and other cryptic taxa that previously

(e.g. individual toxicity tests or population growth) may be more required a high level of taxonomic expertise and sampling effort can

useful indicator of ecosystem health and possibly useful as ‘early be included in more comprehensive ecosystem health assessments

warning’ management tools to prevent ecosystem degradation in the future.

(Corsi et al., 2003). However, there are so few ecosystem health Thirty-ﬁve studies (two estuarine and 33 freshwater) included

assessments done at the individual and population level and even measures of ecosystem processes (e.g. productivity, respiration,

fewer across multiple levels of biological organization, so making photosynthesis, litter breakdown). Although the effects of anthro-

informed decisions about the most relevant indicators to use in pogenic stressors on ecosystem functioning has been demonstrated

ecosystem health assessments is difﬁcult. Understanding the links (Johnston et al., 2015a) and the importance of including meas-

between different levels of biological organization rather than sim- ures of ecosystem function in monitoring programs documented

ply extrapolating from one level to another continues to be an area (Palmer and Febria, 2012), our results show there is still an empha-

of research that needs further development (Attrill and Depledge, sis on measuring traditional community structure and composition

1997; O’Brien and Keough, 2014). metrics in particular taxonomic groups (i.e. ﬁsh and macroinverte-

Taxonomic groups used to assess ecosystem health were biased brates). Furthermore, physical and chemical stressors contributing

towards ﬁsh and macroinvertebrates for both estuarine and fresh- to ecosystem decline are often overlooked in ecosystem health

water studies (Fig. 3b). Fish are likely to be responsive to many assessments. For example, we found that few studies measured

environmental changes. For example, abundance, diversity, and contaminants (excluding nutrients) in their assessments of ecosys-

population demographic rates often decrease after changes in ﬂow tem health (3% were from estuarine and 13% from freshwater

magnitude (Poff and Zimmerman, 2010). Macroinvertebrates live systems). Contaminants are likely to be one of the key stressors

in a wide variety of habitats, respond to disturbance, and are likely affecting ecosystem health but they are not monitored in many

to be sensitive to water quality and pollution (Sharley et al., 2008; studies. This may be because contaminants are not speciﬁcally

Townsend et al., 2009). In addition, both of these taxonomic groups deﬁned as a threat and therefore not monitored, or they may be

form the basis for biotic indices used in biomonitoring (e.g. Index omitted from the program due to lack of expertise or high cost

of Biotic Integrity for ﬁsh in the USA, SIGNAL index and AUSRIVAS of sample analysis. However, contamination is recognized as one

for macroinvertebrates in Australia, and biotic indices in estuar- of the major threats to biodiversity worldwide, along with cli-

ies (Pinto et al., 2009)). However, conceptual links between these mate change, habitat loss and exotic species (Lawler et al., 2006).

728 A. O’Brien et al. / Ecological Indicators 69 (2016) 722–729

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