a conceptual management framework for multiple stressor ... · chu, c., j. barker, l. gutowsky and...

A conceptual management framework for multiple stressor interactions in freshwater lakes and rivers

A conceptual management framework for multiple stressor interactions in freshwater lakes and rivers

C. Chu1, J. Barker1, L. Gutowsky1, and D. de Kerckhove1

1 Aquatic Research and Monitoring Section, Ontario Ministry of Natural Resources and Forestry, 2140 East Bank Drive, Peterborough, ON K9L 1Z8

2018

Science and Research Branch Ontario Ministry of Natural Resources and Forestry

© 2018, Queen’s Printer for Ontario Printed in Ontario, Canada

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Cover image: Image shows examples of five key stressors affecting fish and fisheries; climate change, water extraction via irrigation for agriculture, shoreline development in the Great Lakes, zebra mussels, and boating anglers. (Photo credit: climate change - National Oceanic and Atmospheric Administration, water extraction via irrigation for agriculture (cornell.edu), shoreline development in the Great Lakes (conservationhalton.ca), zebra mussels (ontario.ca), and boating anglers (northernontario.travel).

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Cite this report as: Chu, C., J. Barker, L. Gutowsky and D. de Kerckhove. 2018. A conceptual management

framework for multiple stressor interactions in freshwater lakes and rivers. Ontario Ministry of Natural Resources and Forestry, Science and Research Branch, Peterborough, ON. Climate Change Research Report CCRR-47. 25 p. + append.

Summary Freshwater ecosystems are among the most threatened on Earth. The 5 key human-caused pressures are water extraction, habitat degradation (e.g., fragmentation or chemical pollution), overexploitation of fisheries resources, aquatic invasive species, and climate change. Understanding how multiple stressors associated with these pressures interact to affect rivers, lakes, and fishes is integral to successful management and conservation. We reviewed the scientific literature to examine interactions of multiple stressors on fishes in rivers and lakes. Additive interactions occur when stressors sum to negatively affect ecosystems; synergistic interactions are when stressors amplify each other’s negative effects; and antagonistic interactions are when stressors mitigate each other but have an overall negative effect. Ecological surprises occur when stressors interact to positively affect ecosystems. Our results showed that habitat degradation was the most researched pressure, with studies linking warming associated with climate change to sedimentation, acidification, nutrification, or water diversions also being common. Thirty per cent of the summarized interactions were additive, 27% were synergistic, 34% were antagonistic, 6% were ecological surprises, and 2% showed no interactions. However, determining multiple stressor interactions and their effects in freshwater ecosystems is complex. The types of interactions can vary based on the fish species, life stage, indicator, stressor magnitude, and ecosystem studied. We developed a conceptual Driver-Pressure-State-Impact-Response framework to map and incorporate interactions among stressors into fish and freshwater ecosystem management.

Résumé Un cadre conceptuel de gestion des interactions d’agents stressants multiples dans les lacs et les rivières d’eau douce Les écosystèmes d’eau douce comptent parmi les zones les plus menacées de la Terre. Les cinq (5) principales pressions anthropiques sont l’extraction d’eau, la dégradation d’habitat (p. ex. la fragmentation d’habitat ou le déversement de produits chimiques), la surexploitation des ressources halieutiques, les espèces aquatiques envahissantes et le changement climatique. La compréhension de la façon dont l’interaction de plusieurs agents stressants associés à ces pressions a une incidence sur les rivières, les lacs et les poissons est essentielle à la réussite des efforts de gestion et de conservation. Nous avons examiné les ouvrages scientifiques pour examiner l’effet de l’interaction de plusieurs agents stressants sur les poissons dans les rivières et les lacs. Les interactions sont dites additives lorsque la somme des agents stressants a un effet négatif sur les écosystèmes, synergétiques lorsque les agents stressants amplifient les effets négatifs des uns des autres, et antagonistes lorsque les agents stressants s’atténuent les uns les autres tout en ayant un effet négatif en général. Les interactions sont réputées des surprises écologiques lorsque des agents stressants ont, de par leur interaction, un effet positif sur les écosystèmes. Nos résultats ont montré que la dégradation d’habitat était la pression ayant suscité le plus de

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recherches, dont des études où un lien est couramment fait entre le réchauffement lié au changement climatique et la sédimentation, l’acidification, la nutrification ou les déviations de cours d’eau. Trente pour cent (30 %) des interactions résumées étaient additives, 27 %, synergétiques, 34 %, antagonistes, 6 %, des surprises écologiques, et 2 % inexistantes. Toutefois, la détermination des interactions de plusieurs agents stressants et de leurs effets dans les écosystèmes d’eau douce était complexe. Les types d’interactions peuvent varier en fonction de l’espèce de poisson, de l’étape du cycle de vie, de l’indicateur, de l’ampleur de l’agent stressant et de l’écosystème étudié. Nous avons élaboré un cadre conceptuel FPEIR (forces motrices-pression-état-impact-réponse) en vue de cartographier et d’intégrer les interactions entre les agents stressants dans la gestion du poisson et de l’écosystème d’eau douce.

Acknowledgements The authors thank Josh Cornfield and Jenny Gleeson of MNRF’s Priorities and Planning Section for their support of this work. The project was supported through MNRF’s Climate Change Fund 2016-17 facilitated by MNRF’s Priorities and Planning Section. The authors thank Al Dextrase of MNRF’s Natural Heritage Section and Brian Jackson of MNRF’s Northwest Parks Zone for constructive reviews of earlier drafts of this report.

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Contents

Summary .....................................................................................................................iv

Résumé .......................................................................................................................iv

Acknowledgements ...................................................................................................... v

1.0 Freshwater ecosystems at risk ........................................................................... 1

2.0 Single stressor impacts on freshwater ecosystems and fishes ........................... 4

3.0 Stressor interactions in freshwater ecosystems .................................................. 6 3.1 Stressor interactions ................................................................................... 7 3.2 Documented stressor interactions affecting freshwater fishes .................... 8

4.0 Conceptual framework for stressor interactions and freshwater ecosystem management ..................................................................................................... 14

5.0 Conclusions ...................................................................................................... 19

6.0 Literature cited .................................................................................................. 20

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1.0 Freshwater ecosystems at risk Freshwater ecosystems are among the most threatened on Earth as humans expand

their global footprint and demand for this resource (Sanderson et al. 2002, Halpern et al.

2007, Crain et al. 2008). The 5 key pressures humans place on freshwater ecosystems

are water extraction, habitat degradation, overexploitation, invasive species, and climate

change. These pressures occur at local, regional, and global scales (Costello 2015,

Arthington et al. 2016). While their spatial extent, frequency, and magnitude can vary,

their effects on fresh water resources and ecosystems are similar.

Water extraction can reduce availability of habitat for aquatic organisms and decrease

water quality because chemicals that are normally benign may concentrate as the water

is extracted. Canada has an abundance of fresh water with the world’s third largest

renewable freshwater supply. In 2013, the main water users were: electric power

generation, transmission, and distribution (68%); manufacturing (10%); households

(9%); agriculture (5%); and mining and oil/gas extraction (3%; Statistics Canada 2017).

Habitat degradation can be chemical, such as from sewage treatment plants or

industrial activities, or physical, such as river fragmentation due to water power

development or destruction of lakes and rivers through urbanization, mining, or forestry

(MEA 2005, Helfman 2007, Arthington et al. 2016). In North America, habitat

degradation is the primary pressure affecting fish species at risk (Dextrase and Mandrak

2006, Jelks et al. 2008). Overexploitation is the persistent removal of fisheries

resources beyond sustainably harvestable levels. According to global estimates,

fisheries landings from inland waters have increased 400% since 1950, with many

freshwater stocks at risk of collapse (Allan et al. 2005). Human activities have also led

to invasive species being introduced to new aquatic habitats. In Ontario, people have

knowingly and unknowingly introduced many new species, including freshwater fishes,

invertebrates, and plants (Drake and Mandrak 2010), causing harm to native species

and ecosystems (Strayer 2010). Climate change affects many aspects of freshwater

ecosystems and species, including habitat changes, range shifts, and changes in the

timing of fish spawning and migration (Lynch et al. 2016, Myers et al. 2017). Habitat

changes associated with warming climates have also facilitated the establishment of

invasive species in lakes and rivers (Lynch et al. 2016).

Climate Change Research Report CCRR–47 1

Driver-Pressure-State-Impact-Response (DPSIR) frameworks have been adopted by

managers, scientists, and policy makers to guide resource management decisions when

multiple pressures are in play. These frameworks synthesize pathways of effects of

multiple stressors on ecosystems and help users to develop environmental indicators to

inform risk and environmental assessment (Feld et al. 2016, Oesterwind et al. 2016,

Patricio et al. 2016). They can also be used to outline the relationships between socio-

economic and environmental policies and as decision support tools for management

(EEA 1999, Feld et al. 2016).

Here, we describe components of the DPSIR framework with emphasis on freshwater

ecosystems. Drivers are the first component of DPSIR and are the reason(s) for

ecosystem change. They can be human-caused or natural in origin, with the

overarching human-caused driver being the exponentially increasing number of

humans, and our concomitant demands for food, health, and clean water. Natural

drivers can be fire regimes, earthquakes, or volcanic eruptions (Oesterwind et al. 2016).

Pressures are the direct result of a driver, that is, the human actions in response to the

driver that affect aquatic ecosystems or in the case of natural drivers, the effect of the

driver, e.g., loss of forests after a forest fire (Table 1). A complete list of pressures on

terrestrial and aquatic ecosystems can be found at the IUCN Threats Classification

Scheme (IUCN 2017). Stressors are measurable effects resulting from anthropogenic

pressures that adversely affect the composition, structure, or function of ecosystems

(Matthaei et al. 2010, EC 2014, Feld et al. 2016). The terms pressure and stressor are

not interchangeable because a single pressure (e.g., diffuse pollution) can produce

many stressors (e.g., enhanced concentrations of contaminants, phosphorus, or fine

sediments) (Feld et al. 2016). State variables are measurable quantitative or qualitative

indicators that describe the ecosystem or resource of interest. Impacts or effects of

stressors can be evaluated by tracking changes in state indicators, e.g., abundance,

health, or growth of fishes in response to stressors. Responses are management

actions that are implemented to lessen negative state changes or enhance positive

state changes (Oesterwind et al. 2016).

Using agricultural stressors on freshwater lakes and rivers as a hypothetical example,

the DPSIR pathway may unfold like this: driver; human demand for food, can result in a

pressure on freshwater ecosystems through agricultural irrigation that cascades into


stressors such as disruptions of flows and alterations of water budgets in aquatic

ecosystems. This may reduce the availability of fish habitat (state variable) or

concentrate contaminants in water disrupting fish growth and survival (state variables).

These effects on the state variables may trigger a management response such as

restrictions on the timing or amount of water extracted for irrigation (Matthaei et al.

2010, Feld et al. 2016). With these definitions, the DPSIR framework can be

parameterized to map simple and complex multiple stressor interactions and assess

their effects on freshwater ecosystems as well as to evaluate management options.

Table 1. Examples of drivers and pressures affecting freshwater ecosystems worldwide.

Driver Pressure Human demand for fresh water and food

Water extraction for domestic, commercial, and agricultural use

Human demand for housing, sanitation, energy

Point and non-point source pollution from industrial and domestic household activities, physical habitat alteration or degradation associated with fragmentation from water power, and other water management, rural, urban, and suburban development, mining, and forestry

Human demand for food Fisheries overexploitation and bycatch

Human demand for food and pets Fisheries management (stocking)

Intentional or accidental introduction of invasive species or diseases

Transportation and industrial activities Greenhouse gas emissions and climate change

Individual effects of the 5 key pressures on freshwater ecosystems have been well-

researched (e.g., Allan et al. 2005, Myers et al. 2017), but the interactions and

combined effects of multiple stressors are now emerging in the scientific literature

(Ormerod et al. 2010). In this report, we used a scientific literature review of studies

around the world to summarize individual stressor effects on freshwater ecosystems

and fishes, synthesized documented interactive effects of multiple stressors on fishes in

lakes and rivers, and developed a conceptual framework for freshwater ecosystem

management that incorporates interactions among stressors, including climate change.


2.0 Single stressor on freshwater ecosystems and fishes Fishes are good indicators of stressor effects because many species use different

habitats throughout their life cycle; they change habitat use, physiology, growth or

population dynamics in response to stressors; and they are relatively easy to sample

(Cairns et al. 1993, Nõges et al. 2016, Schinegger et al. 2016). Below we describe how

stressors can disrupt 5 important biological and ecological processes in fishes:

assemblage composition, distribution, demography, phenology, and evolution (Lynch et

al. 2016, Urban et al. 2016, Myers et al. 2017).

Assemblage composition is the number and proportion of fish species found in a lake

or river. Changes to assemblages that are associated with stressors include losses of

native species, gains of new species or changes in the relative abundances of existing

species within assemblages. Stressors can also lead to deviations in the competitive or

predatory interactions among species in an assemblage. Distributional changes are

the contraction or expansion of ranges occupied by species as the result of stressors.

Demography is the study of birth rates, death rates, age distributions, and density or

abundance of populations. Stressors that alter demography affect mortality, growth, and

reproduction in fish populations. Stressors that affect phenology alter the timing of key

life history events (spawning or migration) as well as synchrony of predator-prey

dynamics. Evolutionary effects are the selection for certain heritable traits that affect

life history characteristics such as body size and length at maturation or the selection of

genetic strains of species better adapted to stressor conditions.

Pressures affect biological and ecological processes in different ways. Water extraction

and habitat degradation can reduce the quantity and quality of habitat available for fish

species. Their effects are most evident in growth and survival rates, the habitat species

occupy, and in extreme cases the persistence or extirpation of species in the

assemblage (Table 2). They can also lead to evolutionary selection for heritable traits

better adapted to e.g., drought conditions or pollution tolerance. Overexploitation can

also have evolutionary consequences as size-selective mortality and selection can lead

to earlier maturation, increased reproductive investment, reduced post-maturation

growth, and selection for advantageous behavioural traits (Heino et al. 2015). The


introduction of invasive species can change the assemblage or community within a lake

or river, and cause changes in growth and survival rates of fishes as the new species

may disrupt energy transfer through food webs or facilitate habitat changes that affect

the distribution and demographics of fishes (Strayer 2010). Documented evidence of the

effects of climate change on all 5 of the biological and ecological processes of fishes is

growing in the literature (Lynch et al. 2016, Myers et al. 2017; Table 2).

Table 2. Examples of pressures and stressors, and their direct effects on freshwater ecosystems and fishes.

Pressure Stressors on freshwater ecosystem

Direct effects on fishes

Water extraction

• Decrease or change in water quantity

• Decrease in water quality through concentration of contaminants

• Evolution — selection for certain species and traits (e.g., pollution and/or drought tolerance)

• Demography — reduced growth and survival

• Distribution — reduced ranges • Assemblage composition —

species loss, change in proportions of species

Habitat alteration and/or degradation through pollution and/or physical habitat change

• Disruption of flow regimes and water budgets

• Pollution • Physical habitat

modification

• Evolution — selection for certain species and traits (e.g., pollution-tolerant species)

• Demography — decreased growth and survival

• Distribution — contracted species ranges

• Assemblage composition — loss of species, change in proportions of different species

Overexploitation • Unsustainable harvest of fishes and bycatch (accidental catch of non-target species)

• Evolution — selection for certain traits in targeted species

• Demography — reduced survival • Distribution — contraction in

targeted species ranges • Assemblage composition — loss

of targeted species or increase in abundances of target species' prey


Pressure Stressors on freshwater ecosystem

Direct effects on fishes

Aquatic invasive species (AIS)

• Novel harmful species• Change in habitat e.g.,

Dreissenid-inducedoligotrophicationincreases in waterclarity, macrophyte bedcomposition

• Demography — change in growthand survival due to AIS food webdisruption, competition forresources

• Assemblage composition —change in species richness,competition, or predation of nativespecies

• Distribution — expansion of non-native species ranges

Climate change • Change in water temperature, ice cover, flow, and water levels associated with air temperature and precipitation changes

• Phenology — timing ofreproduction and migration,predator-prey asynchrony

• Evolution — selection for certaintraits, hybridization

• Demography — changes ingrowth/survival of differentspecies

• Distribution — contraction orexpansion of species distributions

• Assemblage composition — lossor gain of species, change inproportions of species

3.0 Stressor interactions in freshwater ecosystems

3.1 Stressor interactions

Stressor interactions broadly fall into 4 categories; additive, synergistic, antagonistic, or

ecological surprises (Figure 1). Additive and synergistic interactions produce effects

that are greater than those caused by each stressor individually, and their combined

effects are unidirectional e.g., warming associated with climate change and thermal

effluent. Additive interactions result in changes in state that are the sum of the effects of

the 2 stressors individually. Synergistic interactions are generated when 2 stressors

amplify the effect of each other e.g., multiplicative, such that negative effects of the

stressors are greater than if the 2 stressors were additive. Antagonistic interactions


occur when 2 or more stressors interact to lessen or mitigate their individual effects the

stressors added together. Ecological surprises occur when stressor effects alleviate

each other and have either no cumulative effect or have a positive effect (Folt et al.

1999, Crain et al. 2008, Côté et al. 2016).

Disentangling the interactions and effects of stressors in ecosystems are complicated

for several reasons. First, the sheer number, intensities, and temporal variation among

stressors in human-modified ecosystems can make interactions difficult to quantify (Vye

2015). Second, biotic responses, e.g., biomass or species richness, can vary due to

evolutionarily or ecologically derived tolerances to stressors. Biota may adapt to

stressors, and biotic interactions may change at different stressor levels (Vinebrooke et

al. 2004, Crain et al. 2008, Jackson et al. 2016). Third, interactions and biotic responses

can also be non-linear or lagged (Nõges et al. 2016). Fourth, responses can vary within

and among species, assemblages, and ecosystems e.g., headwaters versus mid-

reaches of rivers (Schinegger et al. 2016).

Figure 1. Possible interactions among stressors (modified from Schinegger et al. 2016).

Determining stressor effects and their interactions requires studies that compare

controls to impacted ecosystems or replicate ecosystems exposed to similar stressors


or gradients of stress, but these are not common in the scientific literature. The most

common analytical approach has been to understand stressor effects one by one then

iteratively combine stressors (e.g., Vonesh et al. 2009, Battarbee et al. 2012, Jackson et

al. 2016). However, meta-analyses are emerging as useful tools to determine multiple

stressor effects (Crain et al. 2008, Downes 2010, Ormerod et al. 2010, Nõges et al.

2016).

3.2. Documented stressor interactions affecting freshwater fishes

We examined 3 recent syntheses so we could generalize about common stressor

interactions affecting freshwater fishes. In a meta-analysis of more than 219

publications, Nõges et al. (2016) found only 8 studies for rivers and 1 for lakes that

examined multiple stressor impacts and interactions on fishes. Three studies reported

additive interactions between climate change and hydrology, climate change and

connectivity, and climate change and biotic interactions (Appendix A). Lange et al.

(2014) and Johnson and Hering (2009) showed no interaction between

hydromorphology (e.g., flow and/or sedimentation) and nutrient enrichment whereas

Marzin et al. (2013) found additive interactions. Wenger et al. (2011b) showed that the

type of interactions among climate, geomorphology, land use (road proximity), and

invasive species (brook trout) stressors were species dependent. Climate,

geomorphology, and brook trout presence interacted synergistically to affect cutthroat

trout distributions. The climate, geomorphology, and land use interaction was additive

for brook trout but antagonistic for bull trout distributions (Wenger et al. 2011b). The

only lake study (Jeppesen et al. 2012) included in Nõges et al. (2016) showed that

interactions between climate warming and water quality depended on the species.

Climate and water quality effects were additive and negatively affected coldwater Arctic

charr but positively affected species such as bream, pike-perch, and shad (Jeppesen et

al. 2012; Appendix A).

Jackson et al. (2016) reviewed 88 papers that summarized 286 responses (e.g.,

biodiversity or abundance changes) of freshwater organisms to multiple stressors. Of

the 88 studies, 21 focused on stressor effects on fishes and revealed that 57% of the


interactions were antagonistic, 10% were additive or synergistic, and 14% showed

reversals or ecological surprises (Appendix A). Stressor pairs were interactions

combining warming, contamination, habitat alteration, ultraviolet exposure, nutrification

or invasive species. Responses were fish condition, physiology, growth, size, biomass,

or abundance. Interaction types were not consistent for any stressor pair, e.g., fish

biomass or abundance responses to habitat alteration and nutrification were

antagonistic in one study but synergistic in another (Appendix A).

Schinegger et al. (2016) examined interactions among hydrological, morphological,

connectivity, and water quality stressor combinations on 22 fish community

measurements in a study of 3105 fish river sites sampled in 14 European countries

(Appendix A). Forty percent of the interactions were additive, 30% were synergistic and

30% were antagonistic, but antagonistic effects were found only in headwaters and

middle segments of rivers. State indicators showing the strongest responses to the

stressors included direct measures of species tolerance to stressors e.g., density of

species intolerant to a) water quality degradation, b) oxygen depletion, and c)

degradation of lotic spawning habitats.

Of all of the interactions summarized in the 3 synthesis studies, 30% were additive, 34%

were antagonistic, 27% were synergistic, 6% were ecological surprises, and 2% showed

no interactions (Table 3). Habitat degradation was the most common pressure studied

via 2-stressor interactions (e.g., interactions between flow regime alterations and

declines in water quality; Figure 2; Table 3). Studies linking climate warming were also

common, with climate change examined along with sedimentation, acidification,

nutrification, or water diversions (Table 3).


Figure 2. Summary of the number of stressor interactions documented in synthesis

studies of pressure and stressor interactions in freshwater lakes and rivers.


Table 3. Summary of stressor interactions observed for fishes in freshwater rivers and lakes.

Stressors Number of stressors

Number of stressor evaluations

Additive Synergistic Antagonistic Ecological surprise

No interaction

Acidification and warming 2 6 2 3 1 NA NA Changes in in-stream cover and hydrology

2 1 NA NA 1 NA NA

Chemical contamination and warming

2 13 2 8 3 NA

Connectivity and flow alteration 2 7 2 2 3 NA NA Connectivity and water quality 2 11 5 3 3 NA NA Detritus and nutrification 2 2 2 NA NA Flow alteration and in-stream habitat alteration

2 2 2 NA NA NA NA

Flow alteration and water quality 2 13 5 5 3 NA Habitat alteration from water extraction and nutrification associated with farming

2 2 1 NA NA NA 1

Hydrological changes and nutrification

2 2 1 NA NA NA 1

In-stream habitat alteration and water quality

2 9 3 4 2 NA NA

Nutrification and warming 2 1 NA NA 1 NA NA Sedimentation and nutrification 2 3 NA NA 3 NA NA Sedimentation and warming 2 1 1 NA NA NA NA Species invasion and warming 2 2 NA NA 1 1 NA Ultraviolet light and warming 2 3 NA NA 3 NA NA Connectivity, flow alteration, and in-stream habitat alteration

3 2 1 1 NA NA NA

Connectivity, flow alteration, and water quality

3 11 3 4 4 NA NA


Stressors Number of stressors

Number of stressor evaluations

Additive Synergistic Antagonistic Ecological surprise

No interaction

Connectivity, in-stream habitat alteration, and water quality

3 5 1 3 1 NA NA

Flow alteration, in-stream habitat alteration, and water quality

3 5 NA 3 2 NA NA

Hydrological and thermal changes, and habitat fragmentation

3 2 2 NA NA NA NA

Hydrological and thermal changes and invasive species

3 1 1 NA NA NA NA

Temperature changes associated with climate change, nutrification, and salinity

3 8 4 NA NA 3 1

Water diversion and flow and temperature changes associated with climate change

3 1 1 NA NA NA NA

Connectivity, flow alteration, in-stream habitat alteration, and water quality

4 5 1 2 2 NA NA

Flow and temperature changes associated with climate change, geomorphology, and invasive species

4 3 1 1 1 NA NA

NA=not applicable


Fish species diversity and abundance (density, biomass, or number of individuals) were

the indicators used most often to evaluate stressor interactions (Figure 3). These were

likely selected because of the relative ease with which the information can be gathered;

species richness is often easier to measure in rivers or lakes than physiological

responses of organisms. The indicators are not completely independent of each other.

Specifically, assemblage changes associated with either the gain or loss of species may

be reflecting changes in survival, distribution, and habitat selection while changes in

abundance and biomass may be reflecting changes in growth, physiology, and survival.

Figure 3. Fish indicators used to examine multiple stressor interactions in rivers and

lakes.

Results from our synthesis show that quantifying, understanding, and predicting

stressor interactions affecting fishes in freshwater ecosystems is complex and difficult.

We found no consistent pattern — additive, antagonistic, or synergistic interactions

varied by species, indicators, stressors, and ecosystems (Appendix A, Table 3). For

example, Lange et al. (2014) found additive interactions between habitat alteration from

water extraction and nutrification associated with farming intensity when brown trout

distributions were examined but no interaction when abundance indicators were

examined (Appendix A). However, we can draw some conclusions about factors to


consider when conducting multiple stressor assessments for freshwater fishes. Chiefly,

interaction types depend on:

1. Species and life stage of interest: Juveniles and adults can respond differently

to stressors given differences in habitat use and prey resources.

2. Characteristics of the study ecosystem: Interactions among stressors can

vary along the river continuum, i.e., interactions in headwaters were sometimes

different from those in the outlet or middle reaches of rivers

3. Indicators: The types of interactions identified can vary based on which

indicators (e.g., biomass, abundance, density, growth or survival) are used to

describe fishes’ response to stressors.

4. Stressors: The same pressure can produce multiple stressors that affect state

variables or indicators in different ways.

We used these findings to build a conceptual framework for multiple stressor

interactions in fresh waters.

4.0 Conceptual framework for stressor interactions and freshwater ecosystem management Complete mitigation of stressors is often not realistic without removal of the

corresponding drivers, e.g., elimination of water extraction for irrigating agricultural fields

is not likely to be an achievable management action without removal of human demand

for food. Therefore, the resource management literature for multiple stressors has

focused on adaptive management actions aimed at minimizing stressor effects.

Although stressor interactions can vary depending on the species, indicator or

ecosystems of interest, the types of interactions can be used to inform adaptive

conservation and management options (Breitburg et al. 1998, Brown et al. 2013,

Jackson et al. 2016).

The Driver-Pressure-State-Impact-Response framework can be used to understand and

map stressor interactions and possible management actions in rivers and lakes. In this

framework, steps 1 and 2 are identification of the anthropogenic drivers and pressures

at play (Figure 4). Step 3 is identifying all of the stressors resulting from the pressures.


Step 4 involves identifying state indicators that are responsive to the stressors. Mark et

al. (2003) provide a list of marine ecosystem indicators that can also be applied in

freshwater ecosystems for multiple stressor assessments (Appendix B). These

indicators should be sensitive to the stressors listed in step 3, and inform management

objectives such as biodiversity conservation, fisheries management, or ecosystem

health assessments.

Approaches for qualitatively and quantitatively describing stressor effects and

interactions include (Figure 4):

1. Review the scientific literature (useful when data are not available for the

ecosystem, indicators and/or stressors of interest)

2. Analyze data from monitoring programs to test hypotheses about stressor

effects and interactions

3. Conduct experiments to examine stressor effects and interactions

4. Use ecological modelling to map the ecosystem and simulate stressor effects

and interactions

After effects and interactions have been identified, appropriate management responses

can be proposed and implemented (Figure 4). Additive interactions for which 2 or more

stressors affect resources in a linear fashion (a+b interaction; Figure 1) can be

managed by focusing on one of the stressors or on the most dominant stressor to

reduce their combined negative effects (Brown et al. 2013; Figure 4). Synergistic

interactions, in which stressors amplify each another’s effect (a*b interaction), can be

managed by controlling the dominant or amplifying stressor. With both of these

approaches, net improvement is expected because one stressor’s negative effects is

reduced or removed.

With antagonistic interactions (one stressor lessens another’s harm), both may need to

be removed or moderated (Brown et al. 2013, Piggott et al. 2015): Removing only one

may allow the other to cause more harm. Stressor interactions leading to ecological

surprises should be monitored and either managed as is or adaptively managed if/when

state changes are seen (Figure 4). If interactions are not detected among the stressors,


Figure 4. Conceptual framework for management of freshwater ecosystems having

multiple stressors and different interactions among stressors.

we recommend trying to mitigate at least one of the stressors. Although there may be

no interaction, the stressors are likely still having negative effects.

We present agricultural stressors on rivers as a hypothetical example of the DPSIR

framework in action (Figure 5). In this case, the driver is human demand for food. The

pressure could be water extraction and habitat change associated with nutrient


enrichment from agricultural fertilizers. For simplicity, we limit the number of stressors to

reduced water flows and reduced water quality. We select fish growth as an indicator.

An analysis of monitoring data from a river in an agricultural region, a similar river with

reduced flows, and another similar river in a near pristine region may indicate that fish

growth is severely reduced in the agricultural river. These results indicate a synergistic

interaction between water flow and water quality with water quality being the dominant

stressor. Mitigating the water quality stressor would be most appropriate management

action. Actions could include increasing buffer widths to reduce nutrient run off into the

river or restrictions on the amount of fertilizer that can be applied to agricultural lands.

We also apply the DPSIR framework to a hypothetical example of a lake ecosystem

with climate change and invasive species pressures (Figure 5). In this scenario, human

transportation and industrial activities have increased greenhouse gas emissions

leading to warmer air temperatures, and a small-bodied invasive fish has been

introduced to the lake. A mesocosm experiment could be conducted to determine how

warmer water temperatures and the presence of the small-bodied invasive fish affect

growth of walleye (a fish species that prefers cool (19-25 °C) water). The results may

show that growth increased with presence of the invasive species only and was reduced

with warmer water temperatures and the invasive species, but walleye in the tank with

warm water and no invasives were the smallest. These results indicate an antagonistic

interaction between warm water and invasive species presence. The appropriate

management action would be control of both stressors. Options could include

eradication of the invasive species and restrictions on surrounding groundwater

withdrawals (Figure 5).


Figure 5. Driver-Pressure-State-Impact-Response framework to determine management options to address multiple stressor interactions associated with (a) agriculture, and (b) climate change and invasive species in freshwater ecosystems.


5.0 Conclusions Understanding the magnitude of effects and how stressors interact is the key to

developing effective management plans, conservation strategies, and climate change

adaptation. Our review highlights the complexity in determining multiple stressor

interactions in freshwater ecosystems that can vary based on the fish species, indicator,

and/or ecosystem of interest. After stressor effects and interactions and appropriate

management action(s) are identified, taking action will depend on whether relevant

legislation, policies, and regulation mechanisms exist.

Most pressures and their negative effects happen at local scales (e.g., point source

pollution) when compared to the effects of climate change. Using simulations of

seagrass populations, Brown et al. (2013) showed that reducing local stressors

delivered gains when climate change and other stressor interactions were additive or

synergistic. However, when climate change and other stressors interacted in an

antagonistic fashion, reducing the local stressor had little effect because the mitigating

effects of the stressors on one another were lost. The authors concluded that if

interactions are antagonistic, managing local stressors may be more effective in areas

of climate refuge. No matter what the interaction type, managing local stresses

interacting with climate change may buy more time to allow evolutionary adaptation,

develop alternative local management actions, or take mitigating actions to combat

multiple stressor effects (Brown et al. 2013).

None of the studies we reviewed incorporated freshwater fisheries overexploitation as a

pressure. This represents a significant gap in the scientific literature. Stressors that

result in demographic changes in fish populations (fish growth, survival, and population

abundance) can be managed by regulating harvest through season length and slot size

regulations. Harvest regulations are aimed at maximizing population growth. Season

lengths can limit harvest during sensitive periods, e.g., spawning, and slot size limits

can protect reproductive adults. We recommend that future research examine the

interactions of multiple stressors including overexploitation on fish and fisheries in

Ontario to identify appropriate fisheries management actions.


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Appendix A. Synthesis of studies examining pressures, stressors, and stressor interactions on fishes in rivers and lakes.

Synthesis study

Original study

Fish species

Ecosystem Pressure Stressor details State indicator Interaction type

Nõges et al. (2016)

Lange et al. (2014)

brown trout (Salmo trutta)

rivers water extraction and habitat change

habitat alteration from water extraction and nutrification associated with farming intensity

distribution additive

Lange et al. (2014)


rivers water extraction and habitat change

habitat alteration from water extraction and nutrification associated with farming intensity

abundance no interaction

Ayllón et al. (2009)


rivers habitat change

changes in in-stream cover and hydrology

habitat selection antagonistic

Walters et al. (2013)

Chinook salmon (juvenile) (Oncorhynchus tshawytscha)

rivers habitat and climate change

water diversion and flow and temperature changes associated with climate change

abundance additive

Falke et al. (2013)



hydrological and thermal changes and habitat fragmentation




hydrological and thermal changes and habitat fragmentation

abundance additive

Wenger et al. (2011b)

cutthroat trout (Oncorhynchus clarkii)

rivers climate change and invasive species

hydrological and thermal changes and invasive species

abundance additive

Johnson and Hering (2009)

fish assemblage


hydrological changes and nutrification

biodiversity no interaction

Marzin et al. (2013)

fish assemblage


hydrological changes and nutrification

biodiversity additive


Synthesis study

Original study

Fish species


Wenger et al. (2011a)

cutthroat trout (Oncorhynchus clarkii)

rivers habitat and climate change and invasive species

flow and temperature changes associated with climate change, geomorphology, and invasive species

distribution synergistic





brook trout (Salvelinus fontinalis)



distribution antagonistic

Jeppesen et al. (2012)

Arctic charr (Salvelinus alpinus)

lakes habitat and climate change

temperature changes associated with climate change, nutrification, and salinity

abundance additive




abundance additive

vendace (Coregonus albula), whitefish (Coregonus lavaretus), and smelt (Osmerus eperlanus)



abundance additive


Synthesis study

Original study

Fish species


vendace (Coregonus albula), whitefish (Coregonus lavaretus), and smelt (Osmerus eperlanus)



abundance no interaction

roach (Rutilus rutilus)



abundance ecological surprise

perch (southern populations) (Perca fluviatilis)



abundance additive

perch (northern populations) (Perca fluviatilis)




bream (Abramis brama), pike-perch (Sander lucioperca), and shad (Alosa alosa)




Jackson et al. (2016)

Dockray et al. (1998)

rainbow trout (Oncorhynchus mykiss)

mesocosm habitat and climate change

acidification and warming physiology additive

Reid et al. (1997)



acidification and warming growth additive

D'Cruz et al. (1998)



acidification and warming physiology antagonistic


Synthesis study

Original study

Fish species


Morgan et al. (1998)



acidification and warming growth synergistic



acidification and warming physiology synergistic



acidification and warming growth synergistic

Wacksman et al. (2006)

bluegill (Lepomis macrochirus) and fathead minnow (Pimephales promelas)

lab habitat change

chemical contamination physiology antagonistic

Lapointe et al. (2011)

fathead minnow (Pimephales promelas)


chemical contamination and warming

physiology ecological surprise

Peuranen et al. (2003)

grayling (Thymallus thymallus)



physiology antagonistic

grayling (Thymallus thymallus)



abundance antagonistic

Wagner et al. (1997)









Qiang et al. (2012)

tilapia (Oreochromis niloticus)




tilapia (Oreochromis niloticus)





Synthesis study

Original study

Fish species


Linton et al. (1998)




physiology synergistic




growth synergistic

Linton et al. (1997)




physiology ecological surprise




growth ecological surprise




physiology synergistic

Pilati et al. (2009)

gizzard shad (adults) (Dorosoma cepedianum)

mesocosm habitat change

detritus and nutrification biomass antagonistic

gizzard shad (adults) (Dorosoma cepedianum)


detritus and nutrification abundance antagonistic

Gonzalez et al. (2010)

gizzard shad (larval fish) (Dorosoma cepedianum)


sedimentation and nutrification

survival antagonistic




growth antagonistic




biomass antagonistic


Synthesis study

Original study

Fish species


Shrimpton et al. (2007)

Chinook salmon (Oncorhynchus tshawytscha)


sedimentation and warming

growth additive

Kuehne et al. (2012)

Chinook salmon (Oncorhynchus tshawytscha)

lab climate change and invasive species

species invasion and warming

behaviour antagonistic

Reese and Harvey (2002)

steelhead (Oncorhynchus mykiss)

mesocosm climate change and invasive species

species invasion and warming

growth ecological surprise

Greig et al. (2012)

fish assemblage


nutrification and warming biomass antagonistic

Jokinen et al. (2011)

Atlantic salmon (Salmo salar)


ultraviolet light and warming


Atlantic salmon (Salmo salar)



growth antagonistic

Lahnsteiner et al. (2011)





Schinegger et al. (2016)

fish assemblage

headwater streams

habitat change

connectivity and flow alteration


fish assemblage

headwater streams

habitat change


density antagonistic

fish assemblage

headwater streams

habitat change


biodiversity antagonistic

fish assemblage

headwater streams

habitat change

connectivity and water quality

density additive

fish assemblage

headwater streams

habitat change



fish assemblage

headwater streams

habitat change




Synthesis study

Original study

Fish species


fish assemblage

headwater streams

habitat change



fish assemblage

headwater streams

habitat change

flow alteration and water quality

biomass additive

fish assemblage

headwater streams

habitat change


biomass synergistic

fish assemblage

headwater streams

habitat change


density additive

fish assemblage

headwater streams

habitat change



fish assemblage

headwater streams

habitat change



fish assemblage

headwater streams

habitat change


biodiversity synergistic

fish assemblage

headwater streams

habitat change

connectivity, flow alteration, and water quality


fish assemblage

headwater streams

habitat change


density additive

fish assemblage

headwater streams

habitat change



fish assemblage

headwater streams

habitat change



fish assemblage

headwater streams

habitat change



fish assemblage

middle reaches of rivers

habitat change


density additive

fish assemblage


habitat change


density synergistic


Synthesis study

Original study

Fish species


fish assemblage


habitat change



fish assemblage


habitat change



fish assemblage


habitat change


biomass additive

fish assemblage


habitat change


biomass synergistic

fish assemblage


habitat change


density additive

fish assemblage


habitat change


density synergistic

fish assemblage


habitat change



fish assemblage


habitat change



fish assemblage


habitat change



fish assemblage


habitat change

flow alteration and in-stream habitat alteration

density additive

fish assemblage


habitat change

flow alteration and in-stream habitat alteration


fish assemblage


habitat change




Synthesis study

Original study

Fish species


fish assemblage


habitat change


density synergistic

fish assemblage


habitat change


biomass additive

fish assemblage


habitat change


biomass synergistic

fish assemblage


habitat change



fish assemblage


habitat change



fish assemblage


habitat change



fish assemblage


habitat change


biomass additive

fish assemblage


habitat change


biomass synergistic

fish assemblage


habitat change



fish assemblage


habitat change



fish assemblage


habitat change



fish assemblage


habitat change

connectivity, flow alteration, and in-stream habitat alteration

density additive


Synthesis study

Original study

Fish species


fish assemblage


habitat change

connectivity, flow alteration, and in-stream habitat alteration


fish assemblage


habitat change


biomass additive

fish assemblage


habitat change


biomass synergistic

fish assemblage


habitat change



fish assemblage


habitat change


density synergistic

fish assemblage


habitat change



fish assemblage


habitat change



fish assemblage


habitat change

connectivity, in-stream habitat alteration, and water quality

biomass additive

fish assemblage


habitat change


biomass synergistic

fish assemblage


habitat change



fish assemblage


habitat change


density synergistic

fish assemblage


habitat change




Synthesis study

Original study

Fish species


fish assemblage


habitat change

flow alteration, in-stream habitat alteration, and water quality

biomass synergistic

fish assemblage


habitat change



fish assemblage


habitat change


density synergistic

fish assemblage


habitat change



fish assemblage


habitat change



fish assemblage


habitat change

connectivity, flow alteration, in-stream habitat alteration, and water quality

biomass synergistic

fish assemblage


habitat change


density additive

fish assemblage


habitat change



fish assemblage


habitat change



fish assemblage


habitat change



fish assemblage

lower reaches habitat change


biomass synergistic


Synthesis study

Original study

Fish species


fish assemblage



density additive

fish assemblage



density synergistic

fish assemblage





Appendix B. A sample suite of indicators that can be used for multiple stressor assessments in freshwater ecosystems (from Mark et al. 2003).


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