ArticlePDF Available

A Critical Assessment of the Ecological Assumptions Underpinning Compensatory Mitigation of Salmon-Derived Nutrients

May 2015
Environmental Management 56(3)

DOI:10.1007/s00267-015-0538-5

Source
PubMed

Authors:

Scott F Collins

Texas Tech University

Amy M. Marcarelli

Michigan Technological University

Mark Wipfli

University of Alaska Fairbanks

We critically evaluate some of the key ecological assumptions underpinning the use of nutrient replacement as a means of recovering salmon populations and a range of other organisms thought to be linked to productive salmon runs. These assumptions include: (1) nutrient mitigation mimics the ecological roles of salmon, (2) mitigation is needed to replace salmon-derived nutrients and stimulate primary and invertebrate production in streams, and (3) food resources in rearing habitats limit populations of salmon and resident fishes. First, we call into question assumption one because an array of evidence points to the multi-faceted role played by spawning salmon, including disturbance via redd-building, nutrient recycling by live fish, and consumption by terrestrial consumers. Second, we show that assumption two may require qualification based upon a more complete understanding of nutrient cycling and productivity in streams. Third, we evaluate the empirical evidence supporting food limitation of fish populations and conclude it has been only weakly tested. On the basis of this assessment, we urge caution in the application of nutrient mitigation as a management tool. Although applications of nutrients and other materials intended to mitigate for lost or diminished runs of Pacific salmon may trigger ecological responses within treated ecosystems, contributions of these activities toward actual mitigation may be limited.

Content uploaded by Scott F Collins

Content may be subject to copyright.

PROFILE

A Critical Assessment of the Ecological Assumptions

Underpinning Compensatory Mitigation of Salmon-Derived

Nutrients

Scott F. Collins

1,4

•Amy M. Marcarelli

•Colden V. Baxter

•Mark S. Wipﬂi

Received: 13 July 2014 / Accepted: 4 May 2015 / Published online: 13 May 2015

ÓSpringer Science+Business Media New York 2015

Abstract We critically evaluate some of the key eco-

logical assumptions underpinning the use of nutrient re-

placement as a means of recovering salmon populations

and a range of other organisms thought to be linked to

productive salmon runs. These assumptions include: (1)

nutrient mitigation mimics the ecological roles of salmon,

(2) mitigation is needed to replace salmon-derived nutri-

ents and stimulate primary and invertebrate production in

streams, and (3) food resources in rearing habitats limit

populations of salmon and resident ﬁshes. First, we call

into question assumption one because an array of evidence

points to the multi-faceted role played by spawning sal-

mon, including disturbance via redd-building, nutrient re-

cycling by live ﬁsh, and consumption by terrestrial

consumers. Second, we show that assumption two may

require qualiﬁcation based upon a more complete under-

standing of nutrient cycling and productivity in streams.

Third, we evaluate the empirical evidence supporting food

limitation of ﬁsh populations and conclude it has been only

weakly tested. On the basis of this assessment, we urge

caution in the application of nutrient mitigation as a

management tool. Although applications of nutrients and

other materials intended to mitigate for lost or diminished

runs of Paciﬁc salmon may trigger ecological responses

within treated ecosystems, contributions of these activities

toward actual mitigation may be limited.

Keywords Oncorhynchus spp. Paciﬁc salmon Atlantic

salmon Stream restoration Nutrient supplementation 

Primary and secondary productivity

Introduction

Over the past century, society has witnessed the precipitous

decline of Paciﬁc salmon (Oncorhynchus spp.) populations

across much of their native ranges as a result of overhar-

vest, habitat degradation, hatchery operations, and hy-

dropower dams (Lichatowich 1999; Montgomery 2003),

with dramatic ecological, socio-economic, and cultural

effects (National Resource Council 1996). Spawning mi-

grations transport large quantities of accrued nutrients and

organic material from marine to freshwater environments

which beneﬁt both aquatic and terrestrial biota (Gende

et al. 2002). Extensive studies of the ecological services

provided by salmon have informed managers and scientists

about their importance to freshwater and terrestrial envi-

ronments (see reviews by Gende et al. 2002; Schindler

et al. 2003; Naiman et al. 2012) and motivated widespread

efforts to restore or mitigate for the loss of salmon.

Negative anthropogenic impacts on populations of

Paciﬁc salmon within the Columbia River basin led to

legislation requiring responsible parties to compensate

through replacement of functions and values, a practice

known as compensatory mitigation (Race and Fonseca

1996; Naiman 2013). The range of measures taken has

been diverse: hatchery supplementation (Waples 1999);

&Scott F. Collins

collscot@isu.edu

Stream Ecology Center, Department of Biological Sciences,

Idaho State University, Pocatello, ID, USA

Department of Biological Sciences, Michigan Technological

University, Houghton, MI, USA

U.S. Geological Survey, Alaska Cooperative Fish and

Wildlife Research Unit, Institute of Arctic Biology,

University of Alaska Fairbanks, Fairbanks, AK, USA

Present Address: Illinois Natural History Survey, Kaskaskia

Biological Station, Sullivan, IL, USA

123

Environmental Management (2015) 56:571–586

DOI 10.1007/s00267-015-0538-5

spilling water at dams (Raymond 1979); diversion from

turbines (Budy et al. 2002); barging of smolts (Ward et al.

1997); commercial, sport, and subsistence ﬁshing restric-

tions and closures; and habitat and nutrient enhancement

(Stockner 2003). Collectively, these actions have been

embraced by industrial and societal stakeholders and are

used to justify the relicensing of the dams that have con-

tributed to the decline of salmon populations, despite the

fact that such ecosystem recovery or restoration measures

are costly, prone to controversy, and have varying degrees

of success (Williams 2008).

One variety of compensatory mitigation that has been

implemented over the past two decades throughout the

Paciﬁc Northwest is nutrient mitigation. Fisheries scientists

recognized early the important role salmon play in trans-

porting nutrients from marine to freshwater ecosystems

(Juday et al. 1932; Nelson and Edmondson 1955). Nutrient

mitigation efforts are rooted in the concept that current

habitats that have lost salmon, principally natal spawning

grounds and rearing lakes, are less productive than when

salmon runs were at historic levels. Therefore, this

framework purports that additions of nutrients are neces-

sary to alter the trajectory of these ecosystems back toward

a state like that which occurred when salmon spawned in

large numbers, and hence, to contribute to conditions

conducive to producing high numbers of juvenile salmon

(Stockner 2003; Hyatt et al. 2004; Compton et al. 2006).

Nutrients are augmented in a number of different forms,

ranging from pelletized and liquid inorganic nutrients, to

pelletized ﬁsh tissue (commonly referred to as salmon

‘‘analog’’) and salmon carcasses that have been translo-

cated (Stockner 2003; Pearsons et al. 2007; Wipﬂi et al.

2010). As the use of these tools has increased, publication

and citation of studies aimed to determine their ecological

effects have also increased (Fig. 1). These studies report a

range of organismal and ecosystem responses to nutrient

mitigation efforts (Janetski et al. 2009; Kohler et al.

2012), raising questions about the efﬁcacy as well as the

assumptions underlying this mitigation practice.

Here, we evaluate the assumptions underlying nutrient

mitigation and identify potential knowledge gaps, incon-

sistencies, and agreements between these assumptions and

current ecological literature (Fig. 2). We identiﬁed three

general assumptions that are made when this mitigation

practice is employed: (1) nutrient mitigation mimics the

broad ecological roles of salmon, (2) mitigation is needed

to replace salmon-derived nutrients to stimulate aquatic

production in streams, and (3) food resources in rearing

habitats limit populations of salmon and resident ﬁshes. To

evaluate these assumptions, we conducted a literature re-

view, identifying studies that quantify the ecological re-

sponses of aquatic ecosystems to natural or artiﬁcial

additions of salmon-derived nutrients (e.g., carcasses, sal-

mon-carcass analogs, inorganic fertilizers) using Web of

Science, Google Scholar, and relevant citations from re-

view articles (Gende et al. 2002; Schindler et al. 2003;

Roni et al. 2008; Janetski et al. 2009). Searches used the

following keywords alone and in combination: marine-

derived, salmon, salmon-derived, subsidy(ies), nutrient,

mitigation). Most of the primary literature cited here fo-

cuses on Paciﬁc salmon in streams and rivers, yet our

conclusions should be pertinent to Atlantic salmon (Salmo

salar) and perhaps to other anadromous species as well

(Guyette et al. 2013). Our intent is to investigate any dis-

parities between the understanding of the ecological role of

salmon and the application of that knowledge by scientists

and resource managers toward mitigating for the loss or

decline of salmon populations. We focus on the inland

stage of salmon life history because it is the target of

restoration efforts via nutrient supplementation, however,

we acknowledge that factors outside the freshwater phase

of salmon’s life history also inﬂuence their populations

(e.g., Hankin and Healey 1986; Coronado and Hilborn

1998).

Assumption 1 Nutrient mitigation mimics the ecological

roles of salmon.

The addition of nutrients to freshwater ecosystems as

a mitigation effort presupposes that nutrient enrichment

takes primacy over other ecological roles played by

salmon, and accurately mimics the functional contribu-

tions of salmon. Below we evaluate this assumption by

addressing 2 questions. First, is nutrient enrichment the

only ecological service provided by salmon? Second, do

mitigation tools mimic the suite of aquatic-terrestrial

linkages that are part of the ecology of naturally

spawning salmon?

Fig. 1 Annual citations of peer-reviewed studies that focused on the

use of salmon-derived nutrient additions to freshwater ecosystems.

Annual citations were identiﬁed using the Web of Science application

572 Environmental Management (2015) 56:571–586

123

Is Nutrient Enrichment the Only Ecological Role

Played by Salmon?

Paciﬁc salmon are important engineers in freshwater

ecosystems, modifying habitat, community structure, and

ecosystem processes through both disturbance and enrich-

ment (Moore and Schindler 2004; Tiegs et al. 2009). For

example, disturbance during redd digging can have strong

short-term and seasonal effects on stream microbes (Holt-

grieve and Schindler 2011; Levi et al. 2013a). Only 8 % of

studies we identiﬁed in our literature review directly

quantiﬁed disturbance by salmon in some fashion

(Table 1). Although natural spawning runs are character-

ized by both disturbance and enrichment, these phenomena

do not always overlap in time or space (i.e., nutrient release

continues long after redds are constructed). Moreover,

these processes are inﬂuenced by species-speciﬁc charac-

teristics including spawning densities or habitat prefer-

ences. For example, dense concentrations of spawning pink

salmon (O. gorbuscha) may have different ecological im-

pacts than do coho salmon (O. kisutch) that spawn more

diffusely in the landscape. In addition, the relationship

between what constitutes enrichment and disturbance is

likely non-linear and dependent upon scale. Disturbance of

the streambed may reduce bioﬁlm biomass (Verspoor et al.

2010,Ru

¨egg et al. 2012), yet reductions in bioﬁlm biomass

can increase bioﬁlm turnover and, hence, the realized

productivity (Cooper 1973; Lamberti and Resh 1983).

Similarly, disturbance may reduce biomass at the local

scale of a redd, but release nutrients and organic matter that

may have consequences downstream (Moore and Schindler

2004).

The ecological impacts of salmon in freshwater

ecosystems are complex, due to their modiﬁcation of

benthic habitats during spawning, and because their energy

and nutrient contributions occur via multiple pathways.

Live salmon excrete metabolic waste (Groot et al. 1995)

and re-suspend adsorbed nutrients from benthic substrates

into the water column in addition to nutrients released

through decomposition of carcasses (Tiegs et al. 2011).

Thus, enrichment can be a protracted phase involving both

living and dead salmon (Tiegs et al. 2009; Janetski et al.

2009). Disturbance by live salmon also modiﬁes benthic

stream characteristics including sediment size, bed load

(Kondolf and Wolman 1993), ﬂocculent transport (Rex and

Petticrew 2008), standing crops of algae and insects

(Peterson and Foote 2000; Moore et al. 2007; Collins et al.

2011), emergence timing of adult aquatic insects (Moore

and Schindler 2010), ecosystem metabolism (Holtgrieve

and Schindler 2011; Levi et al. 2013a), and nutrient

transformations (Levi et al. 2013b). In some instances,

nutrient enrichment and redd-building disturbance interact,

altering ecosystem metabolism and the energy balance of

the stream ecosystem. For example, dense spawning ag-

gregations of sockeye (O. nerka) reduced bioﬁlms and in-

creased nutrient concentrations, switching the metabolic

balance from autotrophic (primary production exceeded

respiration) to strongly heterotrophic (respiration greatly

exceeded primary production; Holtgrieve and Schindler

2011). The physical stream environment and spawner

density (the combination of which may be dictated by

species traits) mediate the short-term net effects of distur-

bance and enrichment through characteristics including

benthic substrate size and hydrology (Janetski et al. 2009;

Verspoor et al. 2010;Ru

¨egg et al. 2012).

Based on the understanding described above, salmon

have ecological roles in streams that extend beyond the

nutrient enrichment associated with the dead bodies of post-

spawning adults, and nutrient mitigation efforts may over-

look these. Disturbance by salmon is an important ecological

process, yet there is little consideration of the contributions

of disturbance in the context of nutrient mitigation practices.

Fig. 2 Tools for mitigation are developed based on underlying

assumptions. If these assumptions are untested then the mitigation

efforts may be ineffective. More importantly, necessary feedbacks do

not take place to better inform the implementation of mitigation.

Instead, ineffective mitigation efforts do little for salmon and further

exacerbate the need for more restoration efforts, resulting in more

mitigation

Environmental Management (2015) 56:571–586 573

123

Table 1 Summary of abiotic and biotic responses to the natural deposition of salmon carcasses and nutrient augmentation experiments

Study System Subsidy Focal response(s) Response variable Conclusion

Holtgrieve

and

Schindler

(2011)

Stream Natural

spawning run

Gross primary

productivity,

ecosystem respiration

Open-channel

metabolism

Strong heterotrophic responses to increased

salmon nutrients and disturbance of stream

benthos

Levi et al.

(2013a)

Stream Natural

spawning run

Gross primary

productivity,

ecosystem respiration

Open-channel

metabolism

Stream GPP varies in response to salmon-

derived nutrient concentrations, land-use

history, spawner density, and reach level

characteristics

Ebel et al.

(2014)

Stream Analog pellet Gross primary

productivity,

ecosystem respiration

Chamber metabolism,

open-channel

metabolism

Whole-stream and benthic primary

productivity increased in streams treated with

high loads of analog pellets, but no effects

were detected at low analog loads

Rae et al.

(1997)

Lake Inorganic

fertilizer

Phytoplankton Biomass Increased phytoplankton biomass after

fertilization efforts

Mitchell

and

Lamberti

(2005)

Artiﬁcial

and

natural

streams

Natural

spawning

run, salmon

carcass

addition

Dissolved nutrients,

periphyton

Concentration,

biomass

Increase in phosphorus and increases in

periphyton during spawning run. Variable

responses in periphyton attributed to

environmental factors

Schuldt and

Hershey

(1995)

Stream Salmon carcass

addition

Dissolved nutrients,

periphyton,

Concentration,

biomass

Decomposing carcasses increased nutrient

concentrations in streams, resulting in

increased periphyton biomass

Collins

et al.

(2011)

Stream Natural

spawning run

Dissolved nutrients,

periphyton

Concentration,

biomass

Spawning salmon increased nutrient

concentrations and heavy disturbance

reduced stream bioﬁlms

Hoyle et al.

(2014)

Stream Inorganic

fertilizer

Dissolved nutrients,

periphyton

Concentration,

biomass

Inorganic fertilizer additions did not increase

nutrient concentrations in the river, however

chlorophyll accrual rates increased

Ambrose

et al.

(2004)

Stream Salmon carcass

addition

Periphyton Biomass Salmon carcasses had little effect on stream

periphyton. Instead, periphyton positively

responded to increased light availability

¨egg et al.

(2011)

Stream Natural

spawning run

Periphyton Concentration,

biomass

Salmon runs alleviated nutrient limitation of

bioﬁlms in streams of southeastern Alaska

¨egg et al.

(2012)

Stream Natural

spawning run

Periphyton Concentration,

biomass

Bioﬁlm responses to marine-derived nutrients

vary greatly from stream to stream

Verspoor

et al.

(2010)

Stream Natural

spawning run

Periphyton Concentration,

biomass

A negative relationship was observed between

spawner density and periphyton. A positive

relationship was observed between

periphyton and dissolved phosphorus

Wipﬂi et al.

(1998)

Artiﬁcial

and

natural

streams

Salmon carcass

addition

Periphyton, benthic

invertebrates

Biomass, density Addition of salmon carcasses increased stream

bioﬁlms by 15 times in natural streams and

insect density by 8 and 25 times greater in

artiﬁcial and natural streams, respectively

Chaloner

et al.

(2004)

Stream Natural

spawning run

Periphyton, benthic

invertebrates

Biomass Reaches with salmon carcasses experienced

increased periphyton and chironomidae

midge biomass, and decreased biomass of

certain mayﬂy genera

Kohler

et al.

(2008)

Stream Analog pellet Periphyton, benthic

invertebrates

Abundance, biomass Additions of analog pellets increased biomass

of both periphyton and benthic invertebrates

Bilby et al.

(1996)

Stream Salmon carcass

addition

Periphyton, benthic

invertebrates, ﬁshes

Stable isotope Algae, insects, and ﬁshes were signiﬁcantly

enriched with

N and

Kohler and

Taki

(2010)

Stream Analog pellet Periphyton, benthic

invertebrates

Ordination of response

variables

Ordination analysis indicated visual separation

of data points which resulted from additions

of analog pellets. Separation was driven by

both periphyton and benthic invertebrate

responses to analog additions

574 Environmental Management (2015) 56:571–586

123

Table 1 continued

Study System Subsidy Focal response(s) Response variable Conclusion

Claeson

et al.

(2006)

Stream Salmon carcass

addition

Dissolved nutrients,

periphyton, benthic

invertebrates

Density, stable isotope Ammonium concentrations increased near

salmon carcasses, however bioﬁlms were

highly variable. Invertebrate densities of

select taxa were greatest near salmon

carcasses

Rinella

et al.

(2013)

Stream Natural

spawning run

Dissolved nutrients,

periphyton, benthic

invertebrates,

Salvelinus malma

Concentration, stable

isotope

Marine-derived nutrient signature persisted

within the stream for months in the tissue of

benthic invertebrates and Dolly Varden

Reisinger

et al.

(2013)

Stream Natural

spawning run

Periphyton, O. kisutch Stable isotope Organisms in different streams varied in the

degree to which they utilized marine-derived

carbon and nitrogen

Minshall

et al.

(2014)

Stream Inorganic

liquid

fertilizer

Benthic invertebrates Abundance, biomass Fertilizer additions resulted in a 72 % increase

in abundance and a 48 % increase in the

biomass of benthic insects

Minakawa

et al.

(2002)

Stream Natural

spawning

run, salmon

carcass

addition

Benthic invertebrates Growth, biomass Benthic invertebrates found on salmon carcass

tissue experienced greater rates of growth

Chaloner

and

Wipﬂi

(2002)

Artiﬁcial

and

natural

streams

Natural

spawning

run, salmon

carcass

addition

Benthic invertebrates Abundance, biomass Salmon carcasses were colonized by several

taxa in both artiﬁcial and stream

environments. Numeric and temporal

responses were taxa dependent

Verspoor

et al.

(2011)

Stream Natural

spawning run

Benthic invertebrates Abundance A positive relationship was observed between

aquatic insect abundance and spawner

density 10 months after spawning took place.

These relationships were carry-over effects

from the previous year

Lessard and

Merritt

(2006)

Stream Natural

spawning run

Benthic invertebrates Biomass, density,

richness, diversity

Salmon runs decreased richness and diversity

of aquatic insect communities. Reaches that

experienced salmon spawning had greater

density and biomass of aquatic Diptera

Wipﬂi et al.

(1999)

Artiﬁcial

and

natural

streams

Salmon carcass

addition

Periphyton, benthic

invertebrates

Biomass, density The addition of carcasses to natural and

artiﬁcial streams increased both periphyton

and benthic invertebrates. Effects increased

with spawner densities

Lessard

et al.

(2009)

Stream Natural

spawning run

Benthic invertebrates Production Secondary production increased for

chironomidae midges and decreased for

mayﬂy genera

Johnston

et al.

(1990)

Stream Inorganic

fertilizer

O. mykiss, O. kisutch Growth rate Additions of inorganic fertilizers increased the

weights of steelhead and coho

Kiernan

et al.

(2010)

Artiﬁcial

stream

Salmon carcass

addition

Periphyton, benthic

invertebrates, O.

mykiss

Biomass Variable and modest effect of carcass on

periphyton and invertebrate abundance.

Steelhead trout beneﬁtted more from direct

consumption than indirect pathways

Cram et al.

(2011)

Artiﬁcial

stream

Salmon carcass

addition

Periphyton, O. clarki,

kisutch, Cottus spp.

Biomass, growth Limited evidence of increased periphyton or

resident ﬁsh growth resulting from salmon

carcass additions

Wipﬂi et al.

(2010)

Artiﬁcial

stream

Salmon carcass

addition,

inorganic

fertilizer

Nutrient concentration,

periphyton,

invertebrate, O.

kisutch

Concentration,

biomass, density,

growth, body

condition, lipid

content

Water chemistry and biotic responses were

greatest in salmon carcass treatments.

Salmon carcasses have substantially greater

effects than inorganic fertilizers

Environmental Management (2015) 56:571–586 575

123

Moreover, singular pulses of nutrients added as part of

mitigation actions may not have the same effect as the more

protracted enrichment of natural spawning runs in habitats

that have been disturbed, and the forms of nutrients deliv-

ered as part of mitigation actions may differ considerably

from those associated with natural spawning runs.

Table 1 continued

Study System Subsidy Focal response(s) Response variable Conclusion

Chaloner

et al.

(2002)

Artiﬁcial

and

natural

streams

Natural

spawning

run, salmon

carcass

addition

O. kisutch Stable isotope Bioﬁlm, invertebrate, and coho salmon all

exhibited patterns of the utilization of

marine-derived nutrients

Harvey and

Wilzbach

(2010)

Stream Salmon carcass

addition

O. mykiss Biomass, growth rate,

retention

No effect of carcass addition on biomass,

growth or retention during the winter

Perrin et al.

(2006)

Lake Inorganic

fertilizer

Zooplankton, O. nerka,

O. mykiss

Biomass Nutrient additions increased the biomass of

zooplankton. Larger salmonids were

collected along with reduced abundance of a

non-native ﬁsh

Bilby et al.

(1998)

Stream Salmon carcass

addition

O. kisutch, O. mykiss Density, condition,

stable isotope

Densities of both species increased after

additions of salmon carcasses. Both species

had increased body condition. Diet and

isotope indicate strong utilization of carcass

material

Wilzbach

et al.

(2005)

Stream Salmon carcass

addition

O. clarki, O. mykiss Biomass, density,

growth rate

Total biomass and density of both species

responded to canopy removal, not carcass

additions. Greater differences in growth rate

were observed in removed canopies

Wipﬂi et al.

(2003)

Artiﬁcial

stream

Salmon carcass

addition

O. clarki, Salvelinus

malma

Growth rate Both species exhibited increased rates of

growth following additions of salmon

carcasses

Wipﬂi et al.

(2004)

Artiﬁcial

and

natural

streams

Salmon

carcass,

analog pellet

O. kisutch, O. clarki Condition, production,

lipid content

Coho production and lipid content strongly

responded to additions of both carcasses and

analog pellets. Cutthroat production, lipid

content, and condition were signiﬁcantly

higher in streams treated with analog pellets

Denton

et al.

(2009)

Pond Natural

spawning run

Salvelinus malma Growth rate Direct consumption of salmon tissue and eggs

as well as Diptera maggots resulted in

increased rates of growth

Hicks et al.

(2005)

Pond Salmon carcass

addition

O. kisutch Stable isotope Juvenile coho demonstrated clear patterns of

utilization of marine-derived nutrients in

beaver pond habitats

Lang et al.

(2006)

Pond Natural

spawning

run, salmon

carcass

addition

O. kisutch Growth, body

condition,

outmigration

Variable growth rate and body condition

responses to natural and artiﬁcial deposition

of carcass material. Little evidence of short-

term growth inﬂuencing over-winter survival

and outmigration

Scheuerell

et al.

(2007)

Stream Natural

spawning run

O. mykiss, Thymallus

arcticus

Ration size and energy

intake

Both species substantially increased energy

intake when subsidies of salmon were

available. Differential selection of food

resources were observed

Martin

et al.

(2010)

Stream Analog pellet O. kisutch Diet, condition Direct consumption of analog material plus

increased invertebrate abundance in

treatment diets resulted in improved

condition of coho

Rinella

et al.

(2012)

Stream Natural

spawning run

O. kisutch, Salvelinus

malma

Growth rate, energy

density, stable

isotope

Spawner density inﬂuenced the magnitude of

effect for all response variables. Coho

salmon beneﬁtted more than Dolly Varden

Studies are organized by focal response of each respective study. Conclusion statements are those held by the current authors. Due to space

constraints, conclusions do not reﬂect the full suite for each respective paper

576 Environmental Management (2015) 56:571–586

123

Do Mitigation Tools Mimic the Aquatic-Terrestrial

Linkages by Which Naturally Spawning Salmon

Inﬂuence Ecosystems?

Nutrient mitigation efforts typically focus solely on aquatic

habitats and neglect terrestrial food web pathways. Wildlife

such as mink (Ben-David et al. 1997) and bears (Hilder-

brand et al. 2004) frequently transport salmon carcasses to

the land where they are consumed, assimilated, excreted,

and egested, feeding these organisms and further dispersing

nutrients to riparian and forest habitats (Koyama et al.

2005; Koshino et al. 2013). Once in the riparian zone,

marine-derived nutrients can facilitate growth and shifts in

community composition of riparian plants (Helﬁeld and

Naiman 2001; Hocking and Reynolds 2011), however, the

persistence of these nutrients can be rather short-lived and

patchy (Holtgrieve et al. 2009). Salmon carcasses also

provide a subsidy for terrestrial arthropod communities,

which can rapidly consume and transform salmon tissue

into insect tissue (Meehan et al. 2005; Hocking and

Reimchen 2006; Collins and Baxter 2014). These studies

point to the direct effects salmon carcasses may have in

terrestrial habitats, yet there has been little exploration of

the consequences of these effects for food webs in adjacent

habitats.

The effects of salmon carcasses in riparian habitats may

feedback to inﬂuence organisms in aquatic habitats, in-

cluding ﬁsh. Shifts in vegetation structure, vegetation

quality, and community composition may alter the ﬂux of

organic material and organisms back to the aquatic envi-

ronment. Helﬁeld and Naiman (2001) reported the potential

for positive feedbacks of increased vegetation growth and

arthropod production associated with riparian salmon car-

casses (but see critique by Kirchhoff 2003). Terrestrial

invertebrates comprise an important food resource for ju-

venile salmon (Wipﬂi 1997; Allan et al. 2003; reviewed by

Wipﬂi and Baxter 2010), and the rate of terrestrial inver-

tebrate input and subsequent effects on ﬁsh vary with ri-

parian vegetation composition and structure (Saunders and

Fausch 2012).

Unless explicitly expressed within program proposals, it

is unlikely that nutrient mitigation efforts will address

aquatic-terrestrial pathways. Some riparian vegetation may

beneﬁt from subsurface ﬂows of nutrients added to stream

environments (O’Keefe and Edwards 2003), yet many

other riparian and upland forest plants lack the root struc-

ture to utilize this pathway. Likewise, many riparian or-

ganisms (e.g., terrestrial insects) can utilize salmon

carcasses only if they are exposed or removed from the

stream (Hocking and Reimchen 2006; Collins and Baxter

2014). If salmon carcasses are added to streams as part of a

mitigation program, it is likely that translocation of car-

casses to the adjacent terrestrial environment will occur

naturally by wildlife. Conversely, if the treatment was the

pelletized salmon ‘‘analog’’ (Pearsons et al. 2007), or an

inorganic fertilizer (Stockner 2003; Wipﬂi et al. 2010),

natural transfer to or consumption in the riparian zone may

not occur. Bottom-up effects of salmon-derived subsidies

may also extend to terrestrial habitats via the emergence of

aquatic insects, which have been shown to transfer a very

small proportion of marine-derived nutrients to adjacent

riparian zones (Francis et al. 2006). Indeed, the physical

form of a mitigation tool may determine its range of food

web effects across both aquatic and terrestrial habitats.

Assumption 2 Mitigation is needed to replace salmon-

derived nutrients and stimulate primary and invertebrate

production in streams.

Perhaps the central crux of the nutrient mitigation

problem is linked to the presumption that replacement of

nutrients is needed, and that additional nutrients are nec-

essary to sustain increased primary and secondary pro-

ductivity. We limit our critique of assumption 2 to address

three questions. First, should we expect responses to ad-

ditions of salmon-derived nutrients to be ubiquitous? Se-

cond, how important are salmon to overall ecosystem

nutrient budgets? Third, do additions of nutrients and

carbon increase primary and secondary productivity?

Are the Ecological Effects of Salmon Ubiquitous

and Homogeneous?

A multitude of chemical, physical, and biological condi-

tions can affect the ecological outcome and magnitude of

salmon-derived nutrient effects in freshwater ecosystems

(Wipﬂi et al. 1999). Species-speciﬁc characteristics of

spawning migrations and habitat preferences inﬂuence the

magnitude, timing, and location of subsidy delivery within

the landscape (Janetski et al. 2009). These local patterns

are nested within larger regional patterns across the native

ranges of salmon species, which encompass both geologic

and climatic variability. Responses of dissolved nutrients,

algal biomass, and ﬁsh physiological characteristics to

natural salmon runs vary spatially due to factors such as the

size of salmon runs, stream discharge, and sediment size

(Ambrose et al. 2004; Verspoor et al. 2010;Ru

¨egg et al.

2012). For instance, in a recent meta-analysis, Janetski

et al. (2009) found that smaller sediment sizes were more

prone to negative responses by bioﬁlms and benthic insects

to salmon spawners, whereas larger sediments generally

had positive responses. Taken together, such ﬁndings

suggest that effects of natural salmon runs are not ubiqui-

tous, but subject to local, landscape, and regional inﬂu-

ences (Ru

¨egg et al. 2012; Bellmore et al. 2014). On one

hand, this might mean the efﬁcacy of nutrient mitigation

approaches are likely to vary across the extensive home

Environmental Management (2015) 56:571–586 577

123

range of salmon, with select watersheds beneﬁtting more

than others. On the other hand, there is a tendency for

restoration and mitigation practices to be standardized and

ignore this variation within landscapes (Hilderbrand et al.

2005), which may further contribute to the divergent eco-

logical consequences of salmon runs versus nutrient

amendments discussed above.

How Important are Salmon to Ecosystem Nutrient

Budgets?

Historically, an estimated 160–240 million kg of salmon

biomass annually entered freshwater systems across the

Paciﬁc Northwest, variably apportioned in space and time

throughout the region in association with species-speciﬁc

traits (Gresh et al. 2000). Differences in land-use practices,

geology, physical characteristics, and atmospheric N de-

position inﬂuence the rate of nutrient inputs from the sur-

rounding landscape, such that salmon-derived P and N may

be more important in some watersheds and less in others

(Compton et al. 2006). The annual delivery of these often

limiting nutrients and their immediate and longer term

bioavailability (e.g., short-term leaching, longer term re-

tention of P in bone) ultimately inﬂuences the nutrient

status of recipient ecosystems by inﬂuencing the ratios of N

and P. For example, in tributaries of the Snake and Salmon

Rivers in central Idaho where salmon runs have declined,

bioﬁlms exhibit strong limitation by both N and P (San-

derson et al. 2009; Marcarelli et al. 2014), whereas in other

regions N or P may be the primary nutrient limiting pro-

duction. Salmon deliver N, P, and a variety of other trace

nutrients and minerals to ecosystems, and ultimately may

affect the nutrient limitation status of organisms in re-

cipient ecosystems by inﬂuencing the ratios of available N

and P. Moreover, the effects of delivered nutrients will

vary depending on their form; for example, ammonium-N

excreted during spawning will be much more bioavailable

than P delivered as bone in a salmon carcass. Finally, nu-

trient inputs must also be considered in terms of their

balance against nutrient export, including those from out-

migrating juvenile salmon (Moore et al. 2007; Kohler et al.

2013). For example, Gross et al. (1998) estimated that

historic contributions of phosphorus from sockeye salmon

migrations only comprised 3 % of the total annual P budget

for Redﬁsh Lake (Idaho, USA), in part because of export

by smolts. Scheuerell et al. (2005) estimated that current P

export by juvenile Chinook salmon from the Snake River

basin exceeded return by adults in 12 % of years, but

Kohler et al. (2013) found that this varied on a stream-by-

stream basis and that net export occurred when adult

spawner abundance fell below a certain threshold level.

Freshwater microbes within salmon-rearing streams and

lakes may compensate for nutrient reductions by further

shifting the balance between nutrient inputs and outputs.

Nitrogen ﬁxation by cyanobacteria (Marcarelli et al. 2008)

or by symbionts associated with riparian alder (Helﬁeld

and Naiman 2002) can provide an important and frequently

overlooked source of N to both streams and lakes that may

compensate for decreased N availability from salmon. On

the other hand, returning salmon transport a large amount

of carbon along with nutrients, which may promote the

conditions required for nitrogen loss via denitriﬁcation

(Pinay et al. 2008). Both nitrogen ﬁxation and denitriﬁca-

tion may be altered by patterns of nutrient delivery and

disturbance in response to naturally spawning salmon, as

has been observed for nitriﬁcation (Levi and Tank 2013;

Levi et al. 2013b); based upon our review and to the best of

our knowledge, neither of these microbially mediated nu-

trient transformations have been studied in the context of

salmon nutrient mitigation practices.

Do Additions of Nutrients Increase Primary

and Secondary Productivity?

There is a common perception that reduced salmon mi-

grations have led to a decrease in the in situ productivity of

organisms in freshwater ecosystems, particularly those or-

ganisms that are prey for rearing salmon. Production, by

deﬁnition, is the accumulation of tissue through time (re-

ported in units of g m

-2

year

-1

; Huryn and Wallace 2000).

Often, the terms production or productivity are used in-

terchangeably with standing crop or biomass, however,

these metrics represent different phenomena. Standing crop

is a snapshot of biomass at a given time. In contrast, pro-

duction is the accrual of biomass over a period of time, and

it is common to ﬁnd that relationships between the two are

non-linear (Lobo

´n-Cervia

´et al. 2011). Only 6 % of studies

in our review measured primary productivity, and only 6 %

of studies measured the annual secondary production of

aquatic insects (Table 1). In contrast, approximately 45 and

36 % of studies evaluated standing crop and/or density of

stream bioﬁlms and invertebrates, respectively. Addition-

ally, 43 % of the studies evaluated the effects of salmon

subsidies on stream ﬁshes, primarily at the individual level

(i.e., growth rate), and only 4 % measured the effects on

the density of salmon. In most cases, these responses

(standing crop, density and growth) were quantiﬁed over

short time intervals, although they were typically quanti-

ﬁed in the context of well-constructed study designs (e.g.,

upstream control downstream, replicated streams). Only

rarely did studies ascertain whether effects persisted within

or across years, strongly limiting inferences that can be

drawn regarding production. The inferences that can be

drawn from these short-term measurements may result in

misinterpretation regarding persistence of ecological phe-

nomena. Long-term enrichment studies in other contexts

578 Environmental Management (2015) 56:571–586

123

have demonstrated that changes to the structure of com-

munities of organisms require many years to occur (Slavik

et al. 2004), well beyond the temporal scope of most sal-

mon-derived subsidy studies.

Direct measures of production responses to naturally

spawning salmon are becoming more frequent. For in-

stance, bioturbation of the benthos in streams of Southeast

Alaska decreased net primary production in reaches during

the weeks when salmon were spawning (Holtgrieve and

Schindler 2011; Levi et al. 2013a). Consequently, during

these periods in these reaches, respiration from both sal-

mon and benthic heterotrophs exceeded primary produc-

tivity (Holtgrieve and Schindler 2011), however, these

effects appeared to depend on spawner density (Levi et al.

2013a). To our knowledge, secondary production of the

invertebrate assemblage of salmon-rearing streams has

been estimated in only three cases (Lessard et al. 2009;

Bellmore et al. 2012,2013). In streams of Southeast

Alaska, invertebrate production was measured for a subset

of dominant aquatic insects, and mayﬂy production was

generally lower in reaches that received salmon, whereas

production of Chironomidae midges was higher (Lessard

et al. 2009). This ﬁnding suggests that annual production of

aquatic invertebrates does not necessarily and uniformly

increase with spawning salmon.

The limited number of primary and secondary produc-

tion estimates across the home range of salmon, par-

ticularly in regions wherein nutrient mitigation is ongoing

or proposed, signiﬁes a serious empirical weakness un-

derpinning assumption 2, and, hence, the rationale for these

management practices. There is a need to evaluate re-

sponses of biomass and production of all trophic levels

over longer time periods to better understand not only

whether salmon-derived subsidies have effects, but more

importantly how large these effects are and for how long

they persist.

Assumption 3 Food resources in rearing habitats limit

populations of salmon and resident ﬁshes.

In the previous section, we identiﬁed empirical gaps

in the literature regarding primary and secondary pro-

ductivity estimates. The next assumption is that any in-

crease in invertebrate production will be consumed, that

this will translate into higher growth and survival of

salmonids, and, in turn, that this will lead to increases in

salmonid populations (including anadromous and resident

taxa, both of which may be targets for mitigation). Yet,

there is a longstanding debate in ﬁsheries science re-

garding whether rearing salmon and other salmonids are

food limited (Chapman 1966; Mason 1976; Wipﬂi and

Baxter 2010), and evidence suggests that food limitation

may vary according to context (Waters 1988; Huryn

1996; Bellmore et al. 2012). Again, we assess this

assumption by asking three questions. First, what are the

sources of food that sustain salmon and resident ﬁshes?

Second, do responses by individuals (e.g., growth rate,

condition) translate to responses at population levels?

Third, does productivity of rearing habitats relate to the

population dynamics of naturally spawning salmon over

long time scales?

What are the Sources of Food that Sustain Salmon?

Rearing salmonid ﬁshes obtain food and energy from

multiple pathways including in situ benthic production, as

well as subsidies from terrestrial, estuarine, and marine

environments (Wipﬂi and Baxter 2010). Evaluation of the

production of benthic invertebrates versus demand by ﬁsh

has shown that local invertebrate production is often less

than required to sustain ﬁsh production, highlighting the

importance of these alternative sources of food (Allen

1951; Huryn 1996). Inputs of terrestrial invertebrates are

key energy resources for salmon (Wipﬂi 1997; Allan et al.

2003). Headwater tributaries also subsidize salmon with

drifting benthic insects and organic matter (Wipﬂi and

Gregovich 2002; Piccolo and Wipﬂi 2002). Rearing salmon

directly consume high-quality marine subsidies delivered

by the previous generation of spawners, including eggs,

muscle tissue, and emerging fry (Scheuerell et al. 2007;

Denton et al. 2009; Wipﬂi and Baxter 2010) and indirectly

through benthic insect and terrestrial pathways. However,

increased invertebrate productivity may not positively af-

fect ﬁsh if it is manifested in non-drifting or predator re-

sistant taxa or if it is generated in habitats where ﬁsh do not

forage. Recent investigations of invertebrate production

and food demand by ﬁsh populations, including juvenile

salmon, were conducted in main channel and ﬂoodplain

side channel habitats of rivers in Idaho and Washington

where salmon and steelhead runs are small compared to

historic levels, and revealed that invertebrate production in

these habitats generally exceeded ﬁsh demand (Bellmore

et al. 2012,2013).

The extent to which nutrient mitigation actions may

inﬂuence the ﬂow of energy to rearing salmonids through

aquatic and terrestrial pathways likely varies depending on

the form of mitigation tools applied. For instance, liquid or

inorganic fertilizers may inﬂuence only bottom-up path-

ways, whereas analog pellets and carcasses affect both

bottom-up and direct consumption pathways (Fig. 3).

Stream ﬁshes that directly consume salmon subsidies may

be more strongly affected than those receiving salmon

nutrients through indirect pathways due to greater

stoichiometric similarities between living ﬁsh tissue and

salmon carcass tissue and more efﬁcient ﬂow of energy

through fewer trophic levels (Johnson and Ringler 1979;

Scheuerell et al. 2007; Denton et al. 2009).

Environmental Management (2015) 56:571–586 579

123

Do Responses by Individual Fishes Translate to the

Population Level?

Nutrient mitigation aims to increase populations of ﬁshes,

however, most studies quantify responses at the individual

level. In our literature review, studies that quantiﬁed ﬁsh

responses to artiﬁcially placed salmon carcasses, salmon

analog pellets, inorganic fertilizers, and naturally deposited

salmon revealed that approximately 65 % evaluated indi-

vidual growth rates, condition, or other physiological

metrics (Table 1). Salmon smolts and resident ﬁshes ex-

hibit increased growth rates and condition when salmon-

derived subsidies are available (Wipﬂi et al. 2003;

Scheuerell et al. 2007; Kiffney et al. 2014), though not in

all cases (Shaff and Compton 2009; Harvey and Wilzbach

2010). Direct consumption of salmon carcass and salmon

carcass analog material greatly increases energy intake,

resulting in increased growth and/or condition (Scheuerell

et al. 2007; Martin et al. 2010).

Although positive responses to salmon-derived mate-

rials may be detected at the individual level, the magni-

tude of these responses may not translate simply to

inﬂuence the dynamics of populations. The mechanisms

that link these levels are complex, especially for organ-

isms with complicated life histories like salmon, and de-

pend on increased survival throughout the salmon’s life

cycle and increased fecundity (Chapman 1966). While

individual juvenile salmon may grow more if they are fed

more over some time period (e.g., Mason 1976), many

other physical and biological factors may act to constrain

Fig. 3 a The ﬂow of energy

and nutrients from salmon

carcasses is complex. Salmon

subsidies directly inﬂuence

stream consumers like ﬁshes

through the consumption of

ﬂesh, eggs, and milt. These

subsidies can also indirectly

beneﬁt in-stream consumers

through aquatic (e.g., algae,

larval, and adult insects) and

terrestrial pathways (e.g.,

terrestrial arthropods). Salmon

carcasses removed to adjacent

terrestrial habitats also beneﬁt a

suite of terrestrial plants,

insects, and animals. bFish and

aquatic invertebrates also

directly consume salmon

carcass analog (i.e., pelletized

salmon tissue), however, analog

pellets are not removed to

adjacent riparian and upland

forest habitats, though terrestrial

environments may beneﬁt via

insect emergence. cInorganic

fertilizers (e.g., liquid drip,

pellet) are neither directly

consumed by in-stream

consumers nor removed to

adjacent terrestrial habitats, but

may inﬂuence terrestrial

environments via insect

emergence

580 Environmental Management (2015) 56:571–586

123

the expression of this growth in terms of population dy-

namics, ranging from conditions for over-wintering in

freshwater, to outmigration to the ocean. Determining

whether ﬁsh populations respond to salmon nutrients

added either via naturally spawning ﬁsh or as nutrient

mitigation requires long-term, multi-generation studies,

whereas most studies we reviewed measured responses

\1–3 years.

Does Productivity of Rearing Habitats Relate

to the Population Dynamics of Naturally Spawning

Salmon Over Long Time Scales?

Factors that limit populations can be seemingly elusive,

and what may constrain a population in one habitat or time

period may differ in another. The anadromous life histories

of salmon often make it difﬁcult to understand the factors

that limit populations because they occupy multiple habitat

types throughout their life history (Rabeni and Sowa 1996;

Budy and Schaller 2007). Factors outside of their fresh-

water phase such as variable oceanic conditions (Paciﬁc

decadal oscillation; Mantua et al. 1997; Coronado and

Hilborn 1998) and harvest (Hankin and Healey 1986) also

greatly inﬂuence their abundance. Studies that have

evaluated population-level responses to additions of nutri-

ents at time scales that encompass the whole-life history of

salmon are limited (Wilson et al. 2003; Slaney et al. 2003;

Ward et al. 2007), yet there is evidence from coastal

streams and lakes that additions of nutrients and

subsequent increases in invertebrate prey base can

positively inﬂuence returns of adult salmon (Table 2).

Strong paleolimnological relationships were observed be-

tween proxies for primary production and sockeye

escapement in Karluk Lake, Alaska (Finney et al. 2000).

Similar analyses of other Alaskan lakes found relationships

between historic marine-derived nutrient inputs and pri-

mary production (inferred via fossil pigments in lake

sediments), however, relationships between primary pro-

ductivity and subsequent salmon production were not de-

tected (Schindler et al. 2005; Brock et al. 2007). Likewise,

stocking-recruitment models have indicated that marine-

derived nutrients can be a poor predictor of sockeye stock

productivity (Uchiyama et al. 2008). The inconsistent re-

lationships reported between productivity of spawning and

rearing habitats and salmon population dynamics suggest

that there is great variability among environments. As ad-

dressed above, we anticipate productivity to vary spatially

as a function of local, landscape, and regional factors (Poff

and Huryn 1998).

Synthesis and Commentary

The ecological effects of salmon migrations are difﬁcult to

fully understand and appreciate, let alone artiﬁcially du-

plicate. Treatment of salmon as units of carbon and che-

micals for the purposes of mitigation can be readily

achieved with a few calculations, yet this abstracts the

Table 2 Summary of studies evaluating the short-term or historic relationships between the delivery of salmon-derived nutrients and pro-

ductivity of recipient lakes and streams

Study System Species Response

variable

Analytical

approach

Conclusion

Finney et al.

(2000)

Lake O. nerka sediment

microfossils

Sediment

chronology

Reduction in salmon population returns from harvest and climate

reduced nutrient loading and subsequent lake productivity

Moore and

Schindler

(2004)

River O. nerka kg N, P Mass-

balance

Systematic variability in nutrients exported by smolts.

Theoretically possible for smolts to export more than adults

import

Schindler et al.

(2005)

Lake O. nerka sediment

N, fossil

pigments

Sediment

chronology

No support for relationship between salmon population dynamics

and primary productivity

Scheuerell and

Williams

(2005)

River O.

tshawytscha

kg P Mass-

balance

Decreased escapement resulted in increased export of P to marine

environment

Brock et al.

(2007)

Lake O. nerka algal d

fossil

pigments

Sediment

chronology

Considerable historic inter-annual variability between marine-

derived nutrients and primary production, suggesting other

potential drivers

Uchiyama

et al. (2008)

Lake O. nerka smolt d

N Ricker

stock-

recruit

model

Marine-derived nutrients were a poor predictor of sockeye stock

productivity

Environmental Management (2015) 56:571–586 581

123

ecological role of salmon to a detriment. This review of

published literature highlighted several key gaps in the

empirical science. Yet, this understanding seems to be

poorly translated into the practice of nutrient enrichment

for mitigation. Disturbance by salmon is an integral eco-

logical process, yet this role is overlooked or downplayed

relative to enrichment effects, in large part because dis-

turbance effects would be difﬁcult to replicate. Subsidy

form (e.g., dissolved nutrients, inorganic pellet, salmon

carcasses) will further determine the number of trophic

levels that are directly or indirectly affected. Alternate and

simpliﬁed subsidy forms like liquid fertilizers have been

developed and used in some cases, yet these forms do not

replicate the full suite of food web interactions in aquatic

and terrestrial environments inﬂuenced by salmon. In order

to be considered ‘‘mitigation,’’ it seems reasonable to ex-

pect that salmon numbers should increase in direct re-

sponse to nutrient additions, particularly in locations where

salmon numbers have declined. Our synthesis shows that

this has more frequently been assumed than tested. For

example, numerous, well-designed studies have demon-

strated that salmon-derived nutrients may increase bioﬁlm

standing crops (but not always, see Ambrose et al. 2004;

Collins et al. 2011), but the question remains, do these

responses produce enough organic matter to signiﬁcantly

impact higher trophic levels? Additionally, we often focus

on benthic invertebrates as the primary food source for

salmonid ﬁshes, but inputs of terrestrially derived inver-

tebrates and the direct consumption of carcass material are

important components of salmon diets and the effect of

nutrient mitigation on this linkage needs to be further ex-

plored (Wipﬂi and Baxter 2010). Moreover, missing from

this framework is any consideration of how local, land-

scape, and regional factors may mediate responses at any

trophic level or consideration of the timing of resource

availability (Wipﬂi and Baxter 2010). Based on the lit-

erature review and arguments laid out here, we judge that

the underlying assumptions of nutrient mitigation are

largely unsupported due to a lack of empirical evidence,

and therefore that scientiﬁc feedback is not occurring that

might inform improved management practices (Walters

and Holling 1990; Fig. 2).

On the basis of our assessment, we recommend caution

in the application of nutrient mitigation as a management

tool. First and foremost, studies are needed to quantify both

primary and secondary production in mitigation and natural

spawning contexts to evaluate the potential for effective

mitigation. The data gap that exists is troubling, given that

much of the conceptual basis for nutrient mitigation de-

pends on productivity. Second, because mitigation is

predicated on the assumption that more resources are

needed to sustain more ﬁsh, more direct tests of this as-

sumption are required (e.g., via estimates of food demand

by ﬁshes versus food availability). Third, programs need to

account for aquatic-terrestrial linkages, which may require

the addition of salmon-derived nutrients to riparian as well

as aquatic habitats (Fig. 3).

Attempting to mitigate without a clear understanding of

the limitations will waste money, time, and other resources.

Concerns of premature institutionalization of nutrient

mitigation may undermine salmon restoration efforts, as

has been observed in other situations where restoration

techniques have been applied with incomplete under-

standing of their effectiveness (Roni et al. 2002). For ex-

ample, the additions of boulders and large woody debris to

retain gravel for spawning habitats are a common tool

(Reeves et al. 1991), yet there have been no thorough

evaluations of whether these additions increase spawning

salmon (reviewed by Roni et al. 2002). Recognition of the

limitations of nutrient mitigation, via data and feedback,

might yield more realistic goals and expectations. In both

science and management, we often distill and simplify

complex natural phenomena like salmon. We may ac-

knowledge these as abstractions (e.g., most scientists and

ﬁsheries managers do not think of salmon as only ‘‘bags of

nutrients’’), but if the evidence supporting these constructs

is not critically examined, ﬁsheries scientists are likely to

err in terms of applying understanding and our decision

making. An overemphasis on the ecological effects of only

the nutrients derived from salmon and the predominance of

a salmon nutrient enrichment paradigm may actually un-

dermine population recovery efforts by diverting limited

management resources from addressing other factors that

may be more important to limiting salmon populations

such as the dams that block salmon migrations.

We conclude with treatment of a ﬁnal, likely con-

tentious, issue. Is it ethical to receive credit for mitigating

if there is reasonable doubt regarding the efﬁcacy of the

mitigation practice in question? Simply put, as a scientiﬁc

community, do we recognize the addition of nutrients as an

acceptable means of mitigating for loss or reduction of real

salmon runs if we have reason to suspect that the broader

ecological roles of salmon are not mimicked or salmon

populations may not recover by these actions? It is the

responsibility of state, federal, and tribal parties to accu-

rately deﬁne mitigation based on current scientiﬁc evi-

dence. Loosely deﬁning or interpreting a term like

‘‘mitigation’’ undermines attempts to hold accountable

parties that have had detrimental effects on resources like

salmon and their ecosystems, which is contrary to the in-

tent of mitigation policies. As stewards of natural re-

sources, scientists and managers must continually ensure

that mitigation and, more broadly, salmon restoration ad-

here to current scientiﬁc understanding (Lichatowich and

Williams 2009), that we recognize and question our as-

sumptions and even the associated measures and language

582 Environmental Management (2015) 56:571–586

123

we choose to use, and that we ask ourselves the kinds of

questions raised here (Moore and Moore 2013). Nutrient

mitigation as a recovery strategy appears to provide an

incomplete solution to a complex problem, and may divert

focus from larger impediments that could be limiting sal-

mon recovery. From our critique and review, we conclude

that there is substantial doubt as to whether or not com-

pensatory mitigation of salmon-derived nutrients should be

credited as such, and that key uncertainties must be ad-

dressed if it is to be judged a viable mitigation approach.

Acknowledgments We thank the many people whose hard work

and research inﬂuenced the content of this paper. We thank James

Bellmore, Phil Roni, Gordon Holtgrieve, and an anonymous reviewer

for providing constructive and insightful review of this manuscript.

This review was funded by the Bonneville Power Administration

(2007-332-00), Idaho Department of Fish and Game, and Idaho

Power. The use of trade names or products does not constitute en-

dorsement by the U.S. Government.

References

Allan JD, Wipﬂi MS, Caouette JP, Prussian A, Rodgers J (2003)

Inﬂuence of streamside vegetation on inputs of terrestrial

invertebrates to salmonid food webs. Can J Fish Aquat Sci

60:309–320

Allen KR (1951) The Horokiwi stream: a study of a trout popula-

tion. New Zealand Depart Fish Bull 10:1–238

Ambrose HE, Wilzbach MA, Cummins KW (2004) Periphyton

response to increased light and salmon carcass introduction in

northern California streams. J N Am Benthol Soc 23:701–712

Bellmore JR, Baxter CV, Ray AM, Denny L, Tardy K, Galloway E

(2012) Assessing the potential for salmon recovery via ﬂood-

plain restoration: a multitrophic level comparison of dredge-

mined to reference segments. Environ Manag 49:734–750

Bellmore JR, Baxter CV, Martens K, Connolly PJ (2013) The

ﬂoodplain food web mosaic: a study of its importance to salmon

and steelhead with implications for their recovery. Ecol Appl

23:189–207

Bellmore JR, Fremier AK, Mejia F, Newsom M (2014) The response

of stream periphyton to Paciﬁc salmon: using a model to

understand the role of environmental context. Freshw Biol

59:1437–1451

Ben-David M, Hanley T, Klein D, Schell D (1997) Seasonal changes

in diets of coastal and riverine mink: the role of spawning Paciﬁc

salmon. Can J Zool 75:803–811

Bilby RE, Fransen BR, Bisson PA (1996) Incorporation of nitrogen

and carbon from spawning coho salmon into the trophic system

of small streams: evidence from stable isotopes. Can J Fish

Aquat Sci 53:164–173

Bilby RE, Fransen BR, Bisson PA, Walter JK (1998) Response of

juvenile coho salmon (Oncorhynchus kisutch) and steelhead

(Oncorhynchus mykiss) to the addition of salmon carcasses to

two streams in southwestern Washington, USA. Can J Fish

Aquat Sci 55:1909–1918

Brock CS, Leavitt PR, Schindler DE, Quay PD (2007) Variable

effects of marine-derived nutrients on algal production in salmon

nursery lakes of Alaska during the past 300 years. Limnol

Oceanogr 52:1588–1598

Budy P, Schaller H (2007) Evaluating tributary restoration potential

for Paciﬁc salmon recovery. Ecol Appl 17:1068–1086

Budy P, Thiede GP, Bouwes N, Petrosky C, Schaller H (2002)

Evidence linking delayed mortality of Snake River salmon to

their earlier hydrosystem experience. N Am J Fish Manage

22:35–51

Chaloner DT, Wipﬂi MS (2002) Inﬂuence of decomposing Paciﬁc

salmon carcasses on macroinvertebrate growth and standing

stock in southeastern Alaska streams. J N Am Benthol Soc

21:430–442

Chaloner DT, Martin KM, Wipﬂi MS, Ostrom PH, Lamberti GA

(2002) Marine carbon and nitrogen in southeastern Alaska

stream food webs: evidence from artiﬁcial and natural streams.

Can J Fish Aquat Sci 59:1257–1265

Chaloner DT, Lamberti GA, Merritt RW, Mitchell NL, Ostrom PH,

Wipﬂi MS (2004) Variation in responses to spawning Paciﬁc

salmon among three south-eastern Alaska streams. Freshw Biol

49:587–599

Chapman DW (1966) Food and space as regulators of salmonid

populations in streams. Am Nat 100:345–357

Claeson SM, Li JL, Compton JE, Bisson PA (2006) Response of

nutrients, bioﬁlm, and benthic insects to salmon carcass addition.

Can J Fish Aquat Sci 63:1230–1241

Collins SF, Baxter CV (2014) Heterogeneity of riparian habitats

mediates responses of terrestrial arthropods to a subsidy of

Paciﬁc salmon carcasses. Ecosphere 5:art 146

Collins SF, Moerke AH, Chaloner DT, Janetski DJ, Lamberti GA

(2011) Response of dissolved nutrients and periphyton to

spawning Paciﬁc salmon in three northern Michigan streams.

J N Am Benthol Soc 30:831–839

Compton JE, Andersen CP, Phillips DL, Brooks JR, Johnson MG,

Church MR, Hogsett ME, Cairns MA, Rygiewicz PT, McComb

BC (2006) Ecological and water quality consequences of

nutrient addition for salmon restoration in the Paciﬁc northwest.

Front Ecol Environ 4:18–26

Cooper DC (1973) Enhancement of net primary productivity by

herbivore grazing in aquatic laboratory microcosms. Limnol

Oceanogr 18:31–37

Coronado C, Hilborn R (1998) Spatial and temporal factors affecting

survival in coho salmon (Oncorhynchus kisutch) in the Paciﬁc

Northwest. Can J Fish Aquat Sci 55:2067–2077

Cram JM, Kiffney PM, Klett R, Edmonds RL (2011) Do fall additions

of salmon carcasses beneﬁt food webs in experimental streams?

Hydrobiologia 675:197–209

Denton KP, Rich HB Jr, Quinn TP (2009) Diet, movement, and

growth of Dolly Varden in response to sockeye salmon subsidies.

Trans Am Fish Soc 138:1207–1219

Ebel JD, Marcarelli AM, Kohler AE (2014) Bioﬁlm nutrient

limitation, metabolism, and standing crop responses to ex-

perimental application of salmon carcass analog in Idaho

streams. Can J Fish Aquat Sci 71:1796–1804

Finney BP, Gregory-Eaves I, Sweetman J, Douglas MSV, Smol JP

(2000) Impacts of climatic change and ﬁshing on Paciﬁc salmon

abundance over the past 300 years. Science 290:795–799

Francis TB, Schindler DE, Moore JW (2006) Aquatic insects play a

minor role in dispersing salmon-derived nutrients into riparian

forests in southwestern Alaska. Can J Fish Aquat Sci

63:2543–2552

Gende SM, Edwards RT, Willson MF, Wipﬂi MS (2002) Paciﬁc

salmon in aquatic and terrestrial ecosystems. Bioscience

52:917–928

Gresh T, Lichatowich J, Schoonmaker P (2000) An estimation of

historic and current levels of salmon production in the Northeast

Paciﬁc ecosystem: evidence of a nutrient deﬁcit in the freshwater

systems of the Paciﬁc Northwest. Fisheries 25:15–21

Groot C, Margolis L, Clark WC (1995) Physiological ecology of

Paciﬁc salmon. University of British Columbia Press, Vancouver

Environmental Management (2015) 56:571–586 583

123

Gross HP, Wurtsbaugh WA, Luecke C (1998) The role of anadro-

mous sockeye salmon in the nutrient loading and productivity of

Redﬁsh Lake, Idaho. Trans Am Fish Soc 127:1–18

Guyette MQ, Loftin CS, Zydlewski J (2013) Carcass analog addition

enhances juvenile Atlantic salmon (Salmo salar) growth and

condition. Can J Fish Aquat Sci 70:860–870

Hankin DG, Healey MC (1986) Dependence of exploitation rates for

maximum yield and stock collapse on age and sex structure of

chinook salmon (Oncorhynchus tshawytscha) stocks. Can J Fish

Aquat Sci 43:1746–1759

Harvey BC, Wilzbach MA (2010) Carcass addition does not enhance

juvenile salmonid biomass, growth, or retention in six north-

western California streams. N Am J Fish Manag 30:1445–1451

Helﬁeld JM, Naiman RJ (2001) Effects of salmon-derived nitrogen on

riparian forest growth and implications for stream productivity.

Ecology 82:2403–2409

Helﬁeld JM, Naiman RJ (2002) Salmon and alder as nitrogen sources

to riparian forests in a boreal Alaskan watershed. Oecologia

133:573–582

Hicks BJ, Wipﬂi MS, Lang DW, Lang ME (2005) Marine-derived

nitrogen and carbon in freshwater-riparian food webs of the

Copper River Delta, southcentral Alaska. Oecologia

144:558–569

Hilderbrand GV, Farley SD, Schwartz CC, Robbins CT (2004)

Importance of salmon to wildlife: implications for integrated

management. Ursus 15:1–9

Hilderbrand RH, Watts AC, Randle AM (2005) The myths of

restoration ecology. Ecol Soc 10:art 19

Hocking MD, Reimchen TE (2006) Consumption and distribution of

salmon (Oncorhynchus spp.) nutrients and energy by terrestrial

ﬂies. Can J Fish Aquat Sci 63:2076–2086

Hocking MD, Reynolds JD (2011) Impacts of salmon on riparian

plant diversity. Science 331:1609–1612

Holtgrieve GW, Schindler DE (2011) Marine-derived nutrients,

bioturbation, and ecosystem metabolism: reconsidering the role

of salmon in streams. Ecology 92:373–385

Holtgrieve GW, Schindler DE, Jewett PK (2009) Large predators and

biogeochemical hotspots: brown bear (Ursus arctos) predation

on salmon alters nitrogen cycling in riparian soils. Ecol Res

24:1125–1135

Hoyle GM, Holderman C, Anders PJ, Shaﬁi B, Ashley KI (2014)

Water quality, chlorophyll, and periphyton responses to nutrient

addition in the Kootenai River, Idaho. Freshw Sci 33:1024–1029

Huryn AD (1996) An appraisal of the Allen paradox in a New

Zealand trout stream. Limnol Oceanogr 41:243–252

Huryn AD, Wallace JB (2000) Life history and production of stream

insects. Annu Rev Entomol 45:83–110

Hyatt KD, McQueen DJ, Shortreed KS, Rankin DP (2004) Sockeye

salmon (Oncorhynchus nerka) nursery lake fertilization: review

and summary of results. Environ Rev 12:133–162

Janetski D, Chaloner D, Tiegs D, Lamberti G (2009) Paciﬁc salmon

effects on stream ecosystems: a quantitative synthesis. Oecologia

159:583–595

Johnson JH, Ringler NH (1979) Predation on Paciﬁc salmon eggs by

salmonids in a tributary of Lake Ontario. G Great Lakes Res

5:177–181

Johnston NT, Perrin CJ, Slaney PA, Ward BR (1990) Increased

juvenile salmonid growth by whole-river fertilization. Can J Fish

Aquat Sci 47:862–872

Juday C, Rich WH, Kemmerer G, Mann A (1932) Limnological

studies of Karluk Lake, Alaska. Fish Bull 12:407–436

Kiernan JD, Harvey BN, Johnson ML (2010) Direct versus indirect

pathways of salmon-derived nutrient incorporation in ex-

perimental lotic food webs. Can J Fish Aquat Sci 67:1909–1924

Kiffney PM, Buhle ER, Naman SM, Pess GR, Klett RS (2014)

Linking resource availability and habitat structure to stream

organisms: an experimental and observational assessment.

Ecosphere 5:39. doi:10.1890/ES13-00269.1

Kirchhoff MD (2003) Effects of salmon-derived nitrogen on riparian

forest growth and implications for stream productivity: com-

ment. Ecology 84:3396–3399

Kohler AE, Taki D (2010) Macroinvertebrate response to salmon

carcass analogue treatments: exploring the relative inﬂuence of

nutrient enrichment, stream foodweb, and environmental vari-

ables. J N Am Benthol Soc 29:690–710

Kohler AE, Rugenski A, Taki D (2008) Stream food web response to

a salmon carcass analogue addition in two central Idaho, USA

streams. Freshw Biol 53:446–460

Kohler AE, Pearsons TN, Zendt JS, Mesa MG, Johnson CL, Connolly

PJ (2012) Nutrient enrichment with salmon carcass analogs in

the Columbia River basin, USA: a stream food web analysis.

Trans Am Fish Soc 141:802–824

Kohler AE, Kusnierz PC, Copeland T, Venditti DA, Denny L, Gable

J, Lewis BA, Kinzer R, Barnett B, Wipﬂi MS (2013) Salmon-

mediate nutrient ﬂux in selected streams of the Columbia River

basin, USA. Can J Fish Aquat Sci 70:502–512

Kondolf GM, Wolman MG (1993) The sizes of salmonid spawning

gravels. Water Resour Res 29:2275–2285

Koshino Y, Kudo H, Kaeriyama M (2013) Stable isotope evidence

indicates the incorporation into Japanese catchments of marine-

derived nutrients transported by spawning Paciﬁc Salmon.

Freshw Biol 58:1864–1877

Koyama A, Kavanagh K, Robinson A (2005) Marine nitrogen in

central Idaho riparian forests: evidence from stable isotopes. Can

J Fish Aquat Sci 62:518–526

Lamberti GA, Resh VH (1983) Stream periphyton and insect

herbivores: an experimental study of grazing by a caddisﬂy

population. Ecology 64:1124–1135

Lang DW, Reeves GH, Hall JD, Wipﬂi MS (2006) The inﬂuence of

fall-spawning coho salmon (Oncorhynchus kisutch) on growth

and production of juvenile coho salmon rearing in beaver ponds

on the Copper River Delta, Alaska. Can J Fish Aquat Sci

63:917–930

Lessard JL, Merritt RW (2006) Inﬂuence of marine-derived nutrients

from spawning salmon on aquatic insect communities in

southeast Alaskan streams. Oikos 113:334–343

Lessard JA, Merritt RW, Berg MB (2009) Investigating the effect of

marine-derived nutrients from spawning salmon on macroinver-

tebrate secondary production in southeast Alaskan streams. J N

Am Benthol Soc 28:683–693

Levi PS, Tank JL (2013) Nonnative Paciﬁc salmon alter hot spots of

sediment nitriﬁcation in Great Lakes tributaries. J Geophys Res

118:436–444

Levi PS, Tank JL, Ru

¨egg J, Janetski DJ, Tiegs SD, Chaloner DT,

Lamberti GA (2013a) Whole-stream metabolism responds to

spawning Paciﬁc salmon in their native and introduced ranges.

Ecosystems 16:1–15

Levi PS, Tank JL, Tiegs SD, Chaloner DT, Lamberti GA (2013b)

Biogeochemical transformation of a nutrient subsidy: salmon,

streams, and nitriﬁcation. Biogeochemistry 113:643–655

Lichatowich JA (1999) Salmon without rivers: a history of the Paciﬁc

salmon crisis. Island Press, Washington, DC

Lichatowich JA, Williams RN (2009) Failures to incorporate science

into ﬁshery management and recovery programs: lessons from

the Columbia River. Am Fish Soc Symp 70:1005–1019

Lobo

´n-Cervia

´J, Gonzalez G, Budy P (2011) Factors driving spatial

and temporal variation in production and production/biomass

ratio of stream-resident brown trout (Salmo trutta) in Cantabrian

streams. Freshwater Biol 56:2272–2287

Mantua NJ, Hare SR, Zhang Y, Wallace JM, Francis RC (1997) A

Paciﬁc interdecadal climate oscillation with impacts on salmon

production. Bull Am Meteorol Soc 78:1069–1079

584 Environmental Management (2015) 56:571–586

123

Marcarelli AM, Baker MA, Wurtsbaugh WA (2008) Is in-stream N

ﬁxation an important N source for benthic communities and

stream ecosystems? J N Am Benthol Soc 27:186–211

Marcarelli AM, Baxter CV, Wipﬂi MS (2014) Nutrient additions to

mitigate for loss of Paciﬁc salmon: consequences for stream

bioﬁlm and nutrient dynamics. Ecosphere 5:69

Martin AE, Wipﬂi MS, Spangler RE (2010) Aquatic community

responses to salmon carcass analog and wood bundle additions in

restored ﬂoodplain habitats in an Alaskan stream. Trans Am Fish

Soc 139:1828–1845

Mason J (1976) Response of underyearling coho salmon to supple-

mental feeding in a natural stream. J Wildl Manag 40:775–788

Meehan EP, Seminet-Reneau EE, Quinn TP (2005) Bear predation on

Paciﬁc salmon facilitates colonization of carcasses by ﬂy

maggots. Am Midl Nat 153:142–151

Minakawa N, Gara RI, Honea JM (2002) Increased individual growth

rate and community biomass of stream insects associated with

salmon carcasses. J N Am Benthol Soc 21:651–659

Minshall GW, Bahman S, Price WJ, Holderman C, Anders PJ, Lester

G, Barrett P (2014) Effects of nutrient replacement on benthic

macroinvertebrates in an ultraoligotrophic reach of the Kootenai

River, 2003–2010. Freshw Sci 33:1009–1023

Mitchell NL, Lamberti GA (2005) Responses in dissolved nutrients

and epilithon abundance to spawning salmon in southeast Alaska

streams. Limnol Oceanogr 50:217–227

Montgomery DR (2003) King of ﬁsh: the thousand-year run of

salmon. Westview Press, Boulder CO

Moore KD, Moore JW (2013) Ecological restoration and enabling

behavior: a new metaphorical lens? Conserv Lett 6:1–5

Moore JW, Schindler DE (2004) Nutrient export from freshwater

ecosystems by anadromous sockeye salmon (Oncorhynchus

nerka). Can J Fish Aquat Sci 61:1582–1589

Moore JW, Schindler DE (2010) Spawning salmon and the phenology

of emergence in stream insects. Proc R Soc B 277:1695–1703

Moore JW, Schindler DE, Carter JL, Fox J, Grifﬁths J, Holtgrieve

GW (2007) Biotic control of stream ﬂuxes: spawning salmon

drive nutrient and matter export. Ecology 88:1278–1291

Naiman RJ (2013) Socio-ecological complexity and the restoration of

river ecosystems. Inland Waters 3:391–410

Naiman RJ, Alldredge JR, Beauchamp DA, Bisson PA, Congleton J,

Henny CJ, Huntly N, Lamberson R, Levings C, Merrill EN

(2012) Developing a broader scientiﬁc foundation for river

restoration: columbia River food webs. Proc Nat Acad Sci

109:21201–21207

National Research Council (US) Committee on Protection, and

Management of Paciﬁc Northwest Anadromous Salmonids

(1996) Upstream: salmon and society in the Paciﬁc Northwest.

National Academies Press

Nelson PR, Edmondson WT (1955) Limnological effects of fertilizing

Bare Lake, Alaska. Fish Bull Fish Wildlife Serv 56:413–436

O’Keefe TC, Edwards RT (2003) Evidence for hyporheic transfer and

removal of marine-derived nutrients in a sockeye stream in

southwest Alaska. In: Stockner JG (ed) Nutrients in salmonid

ecosystems: sustaining production and biodiversity. American

Fisheries Society, Bethesda, pp 99–110

Pearsons TN, Roley DD, Johnson CL (2007) Development of a

carcass analog for nutrient restoration in streams. Fisheries

32:114–124

Perrin CJ, Rosenau ML, Stables TB, Ashley KI (2006) Restoration of

a montane reservoir ﬁshery via biomanipulation and nutrient

addition. N Am J Fish Manag 26:391–407

Peterson DP, Foote CJ (2000) Disturbance of small-stream habitat by

spawning sockeye salmon in Alaska. Trans Am Fish Soc

129:924–934

Piccolo JJ, Wipﬂi MS (2002) Does red alder (Alnus rubra) in upland

riparian forests elevate macroinvertebrate and detritus export

from headwater streams to downstream habitats in southeastern

Alaska? Can J Fish Aquat Sci 59:503–513

Pinay G, O’Keefe TC, Edwards RT, Naiman RJ (2008) Nitrate

removal in the hyporheic zone of a salmon river in Alaska. River

Res Appl 25:367–375

Poff NL, Huryn AD (1998) Multi-scale determinants of secondary

production in Atlantic salmon (Salmo salar) streams. Can J Fish

Aquat Sci 55:201–217

Rabeni CF, Sowa SP (1996) Integrating biological realism into habitat

restoration and conservation strategies for small streams. Can J

Fish Aquat Sci 53:252–259

Race MS, Fonseca MS (1996) Fixing compensatory mitigation: what

will it take? Ecol Appl 6:94–101

Rae RM, Frances RP, Hamilton PB, Ashley KI (1997) Effects of

fertilization on phytoplankton in Kootenay Lake, British

Columbia. Lake Reserv Manag 13:57–66

Raymond HL (1979) Effects of dams and impoundments on

migrations of juvenile Chinook salmon and steelhead from the

Snake River, 1966 to 1975. Trans Am Fish Soc 108:505–529

Reeves GH, Hall JD, Roelofs TD, Hickman TL, Baker CO (1991)

Rehabilitating and modifying stream habitats. In Meehan WR

(ed) Inﬂuences of forest and rangeland management on salmonid

ﬁshes and their habitats. American Fisheries Society, Special

Publication 19, Bethesda, Maryland, pp 519–557

Reisinger AJ, Chaloner DT, Ru

¨egg J, Tiegs SD, Lamberti GA (2013)

Effects of spawning Paciﬁc salmon on the isotopic composition

of biota differ among southeast Alaska streams. Freshw Biol

58:938–950

Rex JF, Petticrew EL (2008) Delivery of marine-derived nutrients to

streambeds by Paciﬁc salmon. Nat Geosci 1:840–843

Rinella DJ, Wipﬂi MS, Stricker CA, Heintz RA, Rinella MJ (2012)

Paciﬁc salmon (Oncorhynchus spp.) runs and consumer ﬁtness:

growth and energy storage in stream-dwelling salmonids

increase with salmon spawner density. Can J Fish Aquat Sci

69:73–84

Rinella DJ, Wipﬂi MS, Walker CM, Stricker CA, Heintz RA (2013)

Seasonal persistence of marine-derived nutrients in south-central

Alaskan salmon streams. Ecosphere 4:122

Roni P, Beechie TJ, Bilby RE, Leonetti FE, Pollock MM, Pess GR

(2002) A review of stream restoration techniques and a

hierarchical strategy for prioritizing restoration in Paciﬁc

Northwest watersheds. N Am J Fish Manag 22:1–20

Roni P, Hanson K, Beechie T (2008) Global review of the physical

and biological effectiveness of stream habitat rehabilitation

techniques. N Am J Fish Manag 28:856–890

¨egg J, Tiegs SD, Chaloner DT, Levi PS, Tank JL, Lamberti GA

(2011) Salmon subsidies alleviate nutrient limitation of benthic

bioﬁlms in southeast Alaska streams. Can J Fish Aquat Sci

68:277–287

¨egg J, ChalonerDT, Levi PS, Tank JL, TiegsSD, Lamberti GA (2012)

Environmental variability and the ecological effects of spawning

Paciﬁc salmon on stream bioﬁlm. Freshw Biol 57:129–142

Sanderson BL, Coe HJ, Tran CD, Macneale KH, Harstad DL,

Goodwin AB (2009) Nutrient limitation of periphyton in Idaho

streams: results from nutrient diffusing substrate experiments.

J N Am Benthol Soc 28:832–845

Saunders WC, Fausch KD (2012) Grazing management inﬂuences the

subsidy of terrestrial prey to trout in central Rocky Mountain

streams (USA). Freshw Biol 57:1512–1529

Scheuerell MD, Williams JG (2005) Forecasting climate-induced

changes in the survival of Snake River spring/summer Chinook

salmon (Oncorhynchus tshawytscha). Fish Oceanogr 14:448–457

Scheuerell MD, Levin PS, Zabel RW, Williams JG, Sanderson BL

(2005) A new perspective on the importance of marine-derived

nutrients to threatened stocks of Paciﬁc salmon (Oncorhynchus

spp.). Can J Fish Aquat Sci 62:961–964

Environmental Management (2015) 56:571–586 585

123

Scheuerell MD, Moore JW, Schindler DE, Harvey CJ (2007) Varying

effects of anadromous sockeye salmon on the trophic ecology of

two species of resident salmonids in southwest Alaska. Freshw

Biol 52:1944–1956

Schindler DE, Scheuerell MD, Moore JW, Gende SM, Francis TB,

Palen WJ (2003) Paciﬁc salmon and the ecology of coastal

ecosystems. Front Ecol Environ 1:31–37

Schindler DE, Leavitt PR, Brock CS, Johnson SP, Quay PD (2005)

Marine-derived nutrients, commercial ﬁsheries, and production

of salmon and lake algae in Alaska. Ecology 86:3225–3231

Schuldt JA, Hershey AE (1995) Effects of salmon carcass decom-

position on Lake Superior tributary streams. J N Am Benthol Soc

14:259–268

Shaff CD, Compton JE (2009) Differential incorporation of natural

spawners vs. artiﬁcially planted salmon carcasses in a stream

food web: evidence from d15 N of juvenile coho salmon.

Fisheries 34:62–72

Slaney PA, Ward BR, Wightman JC (2003) Experimental nutrient

addition to the Keogh River and application to the Salmon River

in Coastal British Columbia. In: Stockner JG (ed) Nutrients in

salmonid ecosystems: sustaining production and biodiversity.

American Fisheries Society, Bethesda, pp 111–126

Slavik K, Peterson B, Deegan L, Bowden W, Hershey A, Hobbie J

(2004) Long-term responses of the Kuparuk River ecosystem to

phosphorus fertilization. Ecology 85:939–954

Stockner JG (2003) Nutrients in salmonid ecosystems: sustaining

production and biodiversity. American Fisheries Society Sym-

posium 34, Bethesda, Maryland

Tiegs SD, Campbell EY, Levi PS, Ru

¨egg J, Benbow ME, Chaloner

DT, Merritt RW, Tank JL, Lamberti GA (2009) Separating

physical disturbance and nutrient enrichment caused by Paciﬁc

salmon in stream ecosystems. Freshw Biol 54:1864–1875

Tiegs SD, Levi PS, Ru

¨egg J, Chaloner DT, Tank JL, Lamberti GA

(2011) Ecological effects of live salmon exceed those of

carcasses during an annual spawning migration. Ecosystems

14:598–614

Uchiyama TU, Finney BP, Adkison MD (2008) Effects of marine-

derived nutrients on population dynamics of sockeye salmon

(Oncorhynchus nerka). Can J Fish Aquat Sci 65:1635–1648

Verspoor J, Braun D, Reynolds J (2010) Quantitative links between

Paciﬁc salmon and stream periphyton. Ecosystems

13:1020–1034

Verspoor JJ, Braun DC, Stubbs MM, Reynolds JD (2011) Persistent

ecological effects of a salmon-derived nutrient pulse on stream

invertebrate communities. Ecosphere 2:art18

Walters CJ, Holling CS (1990) Large-scale management experiments

and learning by doing. Ecology 71:2060–2068

Waples RS (1999) Dispelling some myths about hatcheries. Fisheries

24:12–21

Ward DL, Boyce RR, Young FR, Olney FE (1997) A review and

assessment of transportation studies for juvenile Chinook salmon

in the Snake River. N Am J Fish Manag 17:652–662

Ward BR, Slaney PA, McCubbing DJF (2007) Watershed restoration

to reconcile ﬁsheries and habitat impacts at the Keogh River in

coastal British Columbia. In: Nielsen J, Dodson JJ, Friedland K,

Hamon TR, Musick J, Verspoor E (eds) Reconciling ﬁsheries

with conservation: proceedings of the fourth world ﬁsheries

congress. American Fisheries Society, Bethesda, pp 587–601

Waters T (1988) Fish production-benthos production relationships in

trout streams. Pol Arch Hydrobiol 35:545–561

Williams J (2008) Mitigating the effects of high-head dams on the

Columbia River, USA: experience from the trenches. Hydrobi-

ologia 609:241–251

Wilson GA, Ashley KI, Land RW, Slaney PA (2003) Experimental

enrichment of two oligotrophic rivers in south coastal British

Columbia. In: Stockner JG (ed) Nutrients in salmonid ecosys-

tems: sustaining production and biodiversity. American Fisheries

Society, Bethesda, pp 149–162

Wilzbach MA, Harvey BC, White JL, Nakamoto RJ (2005) Effects of

riparian canopy opening and salmon carcass addition on the

abundance and growth of resident salmonids. Can J Fish Aquat

Sci 62:58–67

Wipﬂi MS (1997) Terrestrial invertebrates as salmonid prey and

nitrogen sources in streams: contrasting old-growth and young-

growth riparian forests in southeastern Alaska, U.S.A. Can J Fish

Aquat Sci 54:1259–1269

Wipﬂi MS, Baxter CV (2010) Linking ecosystems, food webs, and

ﬁsh production: subsidies in salmonid watersheds. Fisheries

35:373–387

Wipﬂi MS, Gregovich DP (2002) Export of invertebrates and detritus

from ﬁshless headwater streams in southeastern Alaska: impli-

cations for downstream salmonid production. Freshw Biol

47:957–969

Wipﬂi MS, Hudson J, Caouette J (1998) Inﬂuence of salmon

carcasses on stream productivity: response of bioﬁlm and

benthic macroinvertebrates in southeastern Alaska, USA. Can J

Fish Aquat Sci 55:1503–1511

Wipﬂi MS, Hudson JP, Chaloner DT, Caouette JP (1999) Inﬂuence of

salmon spawner densities on stream productivity in southeast

Alaska. Can J Fish Aquat Sci 56:1600–1611

Wipﬂi MS, Hudson JP, Caouette JP, Chaloner DT (2003) Marine

subsidies in freshwater ecosystems: salmon carcasses increase

the growth rates of stream-resident salmonids. Trans Am Fish

Soc 132:371–381

Wipﬂi MS, Hudson JP, Caouette JP (2004) Restoring productivity of

salmon-based food webs: contrasting effects of salmon carcass

and salmon carcass analog additions on stream-resident

salmonids. Trans Am Fish Soc 133:1440–1454

Wipﬂi MS, Hudson JP, Caouette JP, Mitchell NL, Lessard JL, Heintz

RA, Chaloner DT (2010) Salmon carcasses increase stream

productivity more than inorganic fertilizer pellets: a test on

multiple trophic levels in streamside experimental channels.

Trans Am Fish Soc 139:824–839

586 Environmental Management (2015) 56:571–586

123

Multiple lines of evidence reveal complex rainbow trout responses to stream habitat enhancements

Article

Full-text available

Jul 2020

• Habitat enhancements seek to ameliorate the detrimental effects of environmental degradation and take many forms, but usually entail structural (e.g. logs, cribs, reefs) or biogenic (e.g. carrion additions, vegetation plantings, fish stocking) augmentations with the intent of increasing fish annual production (i.e. accrual of new fish biomass through time). Whether efforts increase fish production or simply attract fish has long been subject to debate. • Streams of the Pacific Northwest are commonly targeted for habitat enhancements to mitigate for the detrimental effects of dams and other forms of habitat degradation on Pacific salmon. Nutrient mitigation (i.e. the practice of artificially fertilising freshwaters) is a form of biogenic habitat enhancement that attempts to mimic the enrichment effects of a natural Pacific salmon spawning event. This approach assumes nutrient augmentations alleviate nutrient limitation of primary producers and/or food limitation of primary and secondary consumers, culminating in increased fish production. • We conducted a multi‐year manipulative experiment and tracked responses of interior rainbow trout (Oncorhynchus mykiss ) to annual additions of Pacific salmon carcasses as part of an effort to enhance the productivity of salmonid populations in streams where salmon runs have been lost. We employed an integrated approach to partition the mechanisms driving numerical responses of trout populations across timescales, to assess population turnover, and to track responses to habitat enhancements across individual to population level metrics. • Short‐term numerical increases by trout were shaped by immigration and subsequently via retention of individuals within treatment reaches. As trout moved into treated stream reaches, individuals foraged, grew, and subsequently moved to other locations such that short‐term increases in fish numbers did not persist from year to year. All told, additions of salmon carcasses alleviated apparent food limitation and thereby increased secondary production of rainbow trout. However, at an annual time scale, increased production manifested as larger individual fish, not more fish within treated reaches. Fish movements and high population turnover within treated stream reaches apparently led to the subsequent dispersal of increased fish production. • We found multiple lines of evidence that indicated that annual additions of salmon carcasses aggregated rainbow trout and enhanced their annual production. Through this replicated management experiment, we documented dynamic individual and population level responses to a form of stream habitat manipulation across weekly and annual timescales.

Can nutrient additions facilitate recovery of Pacific salmon?

Article

Full-text available

Jun 2020

Multiple restoration actions have been implemented in response to declining salmon populations. Among these is the addition of salmon carcasses or artificial nutrients to mimic marine-derived nutrients historically provided by large spawning runs of salmon. A key assumption in this approach is that increased nutrients will catalyze salmon population growth. Although effects on aquatic ecosystems have been observed during treatments, it is unclear if permanent population increases for salmon will occur. To test this assumption and address associated uncertainties, we linked a food web model with a salmon life cycle model to examine if carcass additions in a river reach would improve conditions for salmon in the long term. Model results confirmed immediate increases in the biomass of periphyton, macroinvertebrates, and fish during carcass additions. In turn, juvenile salmon grew larger and experienced improved freshwater and smolt survival, which translated to a greater number of adults returning to spawn. However, once additions ceased, salmon abundance returned to pre-treatment levels, which, based on our model, is owing to a combination of instream and out-of-basin factors. Overall, results of this work suggest that benefits during carcass and nutrient additions may not translate into persistent productivity of salmon unless additions are sustained indefinitely, or other limiting factors are addressed

Bring out Your Dead: Factors affecting fate of Pacific lamprey carcasses and resource transport to riparian and stream macrohabitats

Article

Full-text available

Apr 2020

• Anadromous fish transport marine‐derived nutrients to freshwaters during spawning migrations with potential implications for stream food webs. While many studies have explored the role of marine‐derived nutrients instream ecosystems (particularly via Pacific salmonids [Oncorhynchus spp.]), relatively few have examined the spatial distribution and patchiness of non‐salmonid fish carcasses or rates of transport to the riparian zone. • We radio‐tagged and released 144 mature Pacific lamprey (Entosphenus tridentatus) prior to spawning and tracked the fate of post‐spawn carcasses in two inland Columbia River basin streams to characterise spatial distribution of carcasses and marine‐derived nutrient deposition. We found that 27 and 40% of lamprey that could be assigned a fate were moved into the riparian zone adjacent to stream segments exhibiting higher velocity conditions with larger substrates. Conversely, lamprey with instream fates were associated with depositional microhabitats and woody debris dams. Estimated carcass loading rates varied by more than an order of magnitude among habitats. These patterns probably reflect a combination of processes influencing the likelihood of carcass removal (e.g. by predators or scavengers, or stranding) and factors affecting the distribution of carcasses remaining within the stream. • Our results demonstrate substantial transport of lamprey carcasses across the stream‐riparian ecotone and a non‐random distribution of carcasses within streams, patterns which probably influence how resources enter stream and riparian food webs. More broadly, the results suggest local and landscape‐scale hydrogeomorphic factors, along with species‐specific traits and phenology, affect the distribution and potential roles of fish carrion in stream food webs.

Light pollution: a landscape-scale issue requiring cross-realm consideration

Article

Full-text available

Jun 2022

Terrestrial, marine and freshwater realms are inherently linked through ecological, biogeochemical and/or physical processes. An understanding of these connections is critical to optimise management strategies and ensure the ongoing resilience of ecosystems. Artificial light at night (ALAN) is a global stressor that can profoundly affect a wide range of organisms and habitats and impact multiple realms. Despite this, current management practices for light pollution rarely consider connectivity between realms. Here we discuss the ways in which ALAN can have cross-realm impacts and provide case studies for each example discussed. We identified three main ways in which ALAN can affect two or more realms: 1) impacts on species that have life cycles and/or stages in two or more realms, such as diadromous fish that cross realms during ontogenetic migrations and many terrestrial insects that have juvenile phases of the life cycle in aquatic realms; 2) impacts on species interactions that occur across realm boundaries, and 3) impacts on transition zones or ecosystems such as mangroves and estuaries. We then propose a framework for cross-realm management of light pollution and discuss current challenges and potential solutions to increase the uptake of a cross-realm approach for ALAN management. We argue that the strengthening and formalisation of professional networks that involve academics, lighting practitioners, environmental managers and regulators that work in multiple realms is essential to provide an integrated approach to light pollution. Networks that have a strong multi-realm and multi-disciplinary focus are important as they enable a holistic understanding of issues related to ALAN.

Food web perspectives and methods for riverine fish conservation

Article

Full-text available

Apr 2022

Food web analyses offer useful insights into understanding how species interactions, trophic relationships, and energy flow underpin important demographic parameters of fish populations such as survival, growth, and reproduction. However, the vast amount of food web literature and the diversity of approaches can be a deterrent to fisheries practitioners engaged in on‐the‐ground research, monitoring, or restoration. Incorporation of food web perspectives into contemporary fisheries management and conservation is especially rare in riverine systems, where approaches often focus more on the influence of physical habitat and water temperature on fish populations. In this review, we first discuss the importance of food webs in the context of several common fisheries management issues, including assessing carrying capacity, evaluating the effects of habitat change, examining species introductions or extinctions, considering bioaccumulation of toxins, and predicting the effects of climate change and other anthropogenic stressors on riverine fishes. We then examine several relevant perspectives: basic food web description, metabolic models, trophic basis of production, mass‐abundance network approaches, ecological stoichiometry, and mathematical modeling. Finally, we highlight several existing and emerging methodologies including diet and prey surveys, eDNA, stable isotopes, fatty acids, and community and network analysis. Although our emphasis and most examples are focused on salmonids in riverine environments, the concepts are easily generalizable to other freshwater fish taxa and ecosystems. This article is categorized under: Water and Life > Nature of Freshwater Ecosystems Water and Life > Conservation, Management, and Awareness Water and Life > Methods

Nutrient limitation in Atlantic salmon rivers and streams: Causes, consequences, and management strategies

Article

Full-text available

Mar 2022
AQUAT CONSERV

1. Freshwater catchments can experience nutrient deficits that result in reduced primary and secondary productivity. The most commonly limiting nutrients are nitrogen and phosphorus, either separately or together. This review considers the impact of increasing nutrient limitation in temperate basin stream and river systems, focusing on upland areas that currently or previously supported wild Atlantic salmon (Salmo salar) populations. 2. Anthropogenic changes to land use and increases in river barriers have altered upland nutrient dynamics, with particular impacts on salmon and other migratory fish species which may be net importers of nutrients to upland streams. Declining salmon populations may further reduce nutrient sources, reducing ecosystem and fisheries productivity below desired levels. 3. Experimental manipulations of nutrient levels have examined the impacts of this cultural oligotrophication. There is evidence that growth and biomass of juvenile salmon can be increased via appropriate additions of nutrients, offering potential as a conservation tool. However, further research is required to understand the long-term effects of these additions on salmon populations and stream ecosystems, and to assess the vulnerability of downstream habitats to eutrophication as a result. 4. Although purposeful nutrient addition with the aim of enhancing and conserving salmonid populations may be justified in some cases, it should be undertaken in an adaptive management framework. In addition, nutrient addition should be linked to nutrient retention and processing, and integrated into large-scale habitat restoration and recovery efforts. 5. Both the scientific and the management community should recognize that the ecological costs and benefits associated with adding nutrients to salmon streams may change in a non-stationary world.

Light pollution: A landscape-scale issue requiring cross-realm consideration

Preprint

Full-text available

Oct 2021

Terrestrial, marine, and freshwater realms are inherently linked through ecological, biogeochemical and/or physical processes. An understanding of these connections is critical to optimise management strategies and ensure the ongoing resilience of ecosystems. Artificial light at night (ALAN) is a global stressor that can profoundly affect a wide range of organisms and habitats and impact multiple realms. Despite this, current management practices for light pollution rarely consider connectivity between realms. Here we discuss the ways in which ALAN can have cross-realm impacts and provide case studies for each example discussed. We identified three main ways in which ALAN can affect two or more realms: 1) impacts on species that have life cycles and/or stages on two or more realms, such as diadromous fish that cross realms during ontogenetic migrations and many terrestrial insects that have juvenile phases of the lifecycle in aquatic realms; 2) impacts on species interactions that occur across realm boundaries, and 3) impacts on transition zones or ecosystems such as mangroves and estuaries. We then propose a framework for cross-realm management of light pollution and discuss current challenges and potential solutions to increase the uptake of a cross-realm approach for ALAN management. We argue that the strengthening and formalisation of professional networks that involve academics, lighting practitioners, environmental managers and regulators that work in multiple realms is essential to provide an integrated approach to light pollution. Networks that have a strong multi-realm and multi-disciplinary focus are important as they enable a holistic understanding of issues related to ALAN.

Beyond “Donors and Recipients”: Impacts of Species Gains and Losses Reverberate Among Ecosystems Due to Changes in Resource Subsidies

Chapter

Oct 2020

Pervasive environmental degradation has altered biodiversity at a global scale. At smaller scales, species extirpations, invasions, and replacements have greatly influenced how ecosystems function and interact by affecting the exchanges of energy, materials, and organisms. In this chapter, we examine how a variety of environmental stressors, and associated species losses and gains, change the exchange of resources (materials or organisms) within and among ecosystems. We specifically consider how changes that occur within an ecosystem may trigger effects that reverberate (e.g., directly, indirectly, and via feedbacks) back and forth across ecological boundaries and propagate to other ecosystems connected via exchanges of materials and organisms. Our synthesis provides cursory overviews of ecosystem “openness” as it has been addressed by community ecologists and the conceptual development of ecological frameworks used to examine resource exchanges between ecosystems. We then describe four case studies and examine how species losses and gains affect food web structure via resource exchanges between ecosystems, with particular emphasis on effects spanning land-water boundaries. Finally, we discuss the need for more complex conceptual treatment of the interconnectedness of food webs among ecosystems.

Links between fluctuations in sockeye salmon abundance and riparian forest productivity identified by remote sensing

Article

Full-text available

Aug 2021

Pacific salmon (Oncorhynchus spp.) carcasses can fertilize riparian forests with marine-derived nutrients when populations make their annual return to natal streams to spawn; however, the strength of this cross-system linkage likely varies substantially among years due to the interannual fluctuations in abundance that characterize most salmon populations. Here, we used a 36-yr time series (1984-2019) of satellite imagery and salmon abundance estimates to assess spatiotemporal associations between forest greenness (a measure of plant productivity) and adult sockeye salmon (Oncorhynchus nerka) abundance in the lower Adams River, British Columbia, Canada. The Adams River sockeye population displays a qua-drennial pattern of abundance, with a dominant cohort that spawns every four years in numbers that are typically two to three orders of magnitude larger than non-dominant cohorts. We found that variation in forest greenness was consistently explained best by models including dominant cohort year, whereas models lacking an index of salmon abundance were the lowest-ranked. Greenness of riparian vegetation increased by an average of 0.015 NDVI units (approximately 1%) in the summer after a dominant cohort return, and this effect on greenness persisted into the subsequent fall (11-13 months after spawning). The positive association between quadrennial pulses of salmon and riparian greenness occurred in plots both within 30 m of the stream and 95-125 m away from the stream, indicating that the spatial extent of fertilization may occur well beyond areas directly adjacent to the riverbank. These results suggest that forests respond to cyclical variation in salmon abundance and that overwinter storage of marine-derived nutrients within catchments allows plants to capitalize on these nutrients in the following growing season. Continued advances in remote sensing technology will enhance our understanding of cross-system resource linkages and can inform the ecosystem-based management of Pacific salmon.

Carcass Additions Influence Food Webs Through Bottom-Up and Direct Consumption Pathways Along a Fish Species Assemblage Gradient

Article

Full-text available

Jan 2021
ECOSYSTEMS

The loss of subsidies delivered by anadromous fish to inland stream ecosystems may have profound influences on stream food webs. However, studies have focused on food web responses in ecosystems where the fish assemblage is dominated by salmonids. We evaluated food web responses to carcass additions in three locations of an interior Columbia River Basin stream with varying native fish assemblages. Periphyton biomass responses were mixed with increases in treatment compared to control reaches of the middle and downstream pairs, but not in the upstream pair where scavenging by bears removed the majority of carcasses. Stable isotope analysis revealed marine-derived nutrient (MDN) enrichment of periphyton and invertebrate functional feeding groups in the middle and downstream pairs (up to 12% MDN derived), but not in the upstream pair. Non-salmonid fish exhibited limited MDN assimilation (~ 5 and 10% MDN derived), with isotopic enrichment patterns similar to lower trophic levels and little evidence of eggs and carcass material consumption, suggesting bottom-up transfer of MDN to non-salmonid fishes. In contrast, across the three study pairs, juvenile Chinook Salmon (Oncorhynchus tshawytscha) and steelhead trout (O. mykiss) assimilated MDN rapidly, obtaining up to 25% and 57% of their nitrogen from carcasses, respectively. Diet analysis and isotopic enrichment patterns indicated that juvenile salmonid assimilation occurred primarily through direct consumption of eggs and carcass tissue. Our findings suggest that salmonids in this region may experience more benefit from carcass additions containing eggs, while non-salmonids are likely to experience minimal MDN incorporation whether or not eggs are present.