The role of winter phenology in shaping the ecology of ... · conditions (e.g. cool short summers,...

OVERVIEW

The role of winter phenology in shaping the ecology of freshwaterfish and their sensitivities to climate change

B. J. Shuter • A. G. Finstad • I. P. Helland •

I. Zweimüller • F. Hölker

Received: 7 November 2011 / Accepted: 4 August 2012 / Published online: 23 August 2012

� Springer Basel AG 2012

Abstract Thermal preference and performance provide

the physiological frame within which fish species seek

strategies to cope with the challenges raised by the low

temperatures and low levels of oxygen and food that

characterize winter. There are two common coping strate-

gies: active utilization of winter conditions or simple

toleration of winter conditions. The former is typical of

winter specialist species with low preferred temperatures,

and the latter is typical of species with higher preferred

temperatures. Reproductive strategies are embodied in the

phenology of spawning: the approach of winter conditions

cues reproductive activity in many coldwater fish species,

while the departure of winter conditions cues reproduction

in many cool and warmwater fish species. This cuing

system promotes temporal partitioning of the food resour-

ces available to young-of-year fish and thus supports

high diversity in freshwater fish communities. If the

zoogeographic distribution of a species covers a broad

range of winter conditions, local populations may exhibit

differences in their winter survival strategies that reflect

adaptation to local conditions. Extreme winter specialists

are found in shallow eutrophic lakes where long periods of

ice cover cause winter oxygen levels to drop to levels that

are lethal to many fish. The fish communities of these lakes

are simple and composed of species that exhibit specialized

adaptations for extended tolerance of very low tempera-

tures and oxygen levels. Zoogeographic boundaries for

some species may be positioned at points on the landscape

where the severity of winter overwhelms the species’

repertoire of winter survival strategies. Freshwater fish

communities are vulnerable to many of the shifts in envi-

ronmental conditions expected with climate change.

Temperate and northern communities are particularly

vulnerable since the repertoires of physiological and

behavioural strategies that characterize many of their

members have been shaped by the adverse environmental

conditions (e.g. cool short summers, long cold winters) that

climate change is expected to mitigate. The responses of

these strategies to the rapid relaxation of the adversities

that shaped them will play a significant role in the overall

responses of these fish populations and their communities

to climate change.

Keywords Thermal performance � Bioenergetics �Survival strategies � Zoogeographic boundaries �Climate change � Winter kill

Introduction

In the northern hemisphere, the time frame that winter

occupies in the annual round of seasons varies widely from

B. J. Shuter

Harkness Laboratory of Fisheries Research,

Ontario Ministry of Natural Resources, Peterborough, Canada

B. J. Shuter

Department of Ecology and Evolutionary Biology, University

of Toronto, 25 Harbord Street, Toronto M5S3G5, Canada

A. G. Finstad � I. P. HellandNorwegian Institute for Nature Research, P.O. Box 5685,

Sluppen, 7485 Trondheim, Norway

I. Zweimüller

Department of Evolutionary Biology, Faculty of Life Sciences,

University of Vienna, Vienna, Austria

F. Hölker (&)Leibniz Institute of Freshwater Ecology and Inland Fisheries,

12587 Berlin, Germany

e-mail: [email protected]

Aquat Sci (2012) 74:637–657

DOI 10.1007/s00027-012-0274-3 Aquatic Sciences

123

place to place and from year to year. This variable ‘phe-

nology’ shapes the annual life cycle of all the organisms

resident in temperate and northern freshwater ecosystems,

for winter is the period of food scarcity and darkness that

follows the summer production pulse (Kalff 2002—pages

140, 323; Suski and Ridgway 2009a, b). For northern

lakes, winter is marked by a period of ice cover. The

physics of ice formation and retreat are relatively well

understood but there is much to learn about the physical

processes operative in the under-ice environment (see

Kirillin et al. 2012). In addition, many aspects of the

under-ice environment have important implications for

limnetic biota: (1) light intensity and water temperature

are at their annual minima and oxygen levels are in

decline; (2) little primary production occurs; (3) the great

majority of biomass available for consumption by fish is

an accumulation from previous summer production pulses;

and (4) the absence of light impedes visual feeders (e.g.

most freshwater fish) from finding the few prey that are

available. Since winter is the season when prey are scarce

(or inaccessible), changes in winter phenology can cause

large changes in fish growth and reproduction. In North

America, the south to north climatic gradient of shorter

summers and longer winters is accompanied by systematic

changes in population characteristics (e.g., spawning time,

somatic growth, size and age at reproduction, lifespan) of

many freshwater fish species (e.g. Dunlop and Shuter

2006; Zhao et al. 2008; McDermid et al. 2010; Venturelli

et al. 2010). Similar links between fish life history char-

acteristics and climate gradients have been noted in

Europe and South America (Heibo et al. 2005; Lappalai-

nen and Tarkan 2007; Finstad et al. 2010), and in marine

fish species (Pörtner 2006).

The characteristics of winter phenology that are of

particular importance for fish are its start and end dates and

its overall duration (e.g. Shuter and Post 1990). To illus-

trate how these characteristics vary geographically, we

adopt the following, somewhat simplistic (but clear and

unambiguous) definition of winter: winter is the period of

ice cover for a water body (lake or river). This definition

provides us with clear measures for winter start, end and

duration. It also isolates those ecosystems that experience

the full set of adverse conditions outlined above, from

those that experience a moderated subset, conditioned by

annual minimum light levels that are not impeded by ice

cover. We use the physical limnological model FLAKE

(Kirillin 2010; Kirillin et al. 2011) and climatic conditions

for the years 2005–6 to illustrate the geography of ‘winter’

conditions for a typical lake, and how that geography dif-

fers between North America and Europe (Fig. 1).

In the present paper, we provide a conceptual overview

of current knowledge on the challenges that winter poses

for temperate freshwater fish. We have based our review on

the authors’ familiarity with the relevant literature, sup-

plemented by a systematic Web of Science search of papers

published from Jan 2006 thru Feb 2012 using topic key

words ‘winter’ and ‘fish’.

We begin by discussing the functional trade-offs faced

by fish that must live with different winter phenologies. We

then give an overview of the bioenergetic context that

defines many of the strategies developed by fish to deal

with winter. We continue by classifying fish species with

respect to their thermal tolerances, link these tolerances to

both winter survival- and reproductive strategies, and

illustrate the potential for intraspecific variation in these

strategies. We show that winter conditions and thermal

tolerances are tightly linked to the zoogeographic bound-

aries of many freshwater fish species and we discuss some

of the processes generating high mortalities at these

boundaries and consequent shifts in fish community com-

position. Finally, we argue that our categorization of winter

survival strategies highlights the relative sensitivities of

different freshwater fish species to climate change and

adds to the growing list of characteristics that make

temperate freshwater ecosystems particularly vulnerable to

the impacts of climate change (Jeppesen et al. 2010;

Woodward et al. 2010).

Fig. 1 Illustration of continental (Europe—stippled vs. North Amer-ica—cross hatched) differences in how latitude influences the start(solid boundary lines) and end (dashed boundary lines) of the icecover period for a typical lake. Day zero is Jan 1. Values were derived

using the physical limnological model FLAKE (Kirillin et al. 2011)

and observed climatic conditions for 2005–6. A lake with mean depth

of 10 m and secchi depth of 2 m was assumed. European regions

reflect variation expected over a range in longitude from 20oE to

30oE; North American regions reflect variation expected over a range

in longitude from -75oW to -100oW

638 B. J. Shuter et al.

123

Winter phenology and fish survival

The challenges of winter

In temperate latitudes, the phenology of the seasons gen-

erates wide annual variation in light, temperature, oxygen

and food resources and this variation poses significant

trade-off challenges (Fig. 2). A common objective for all

species and life stages is to allocate available energy to

maximize individual survival and reproductive success. For

most species, individuals accumulate energy over spring-

summer-fall and deplete it during winter (Shuter and Post

1990). Winter depletion is particularly acute for early life

stages, since the weight-specific capacity to store energy

decreases with decreasing body size, while weight-specific

energy expenditure increases (Shuter and Post 1990; Ultsch

1989). Increased winter mortality, resulting from exhaus-

tion of energy reserves, has been reported among the early

life stages of a wide variety of species (e.g. smallmouth

bass Micropterus dolomieui—Oliver et al. 1979; perch

Perca fluviatilis and flavescens—Post and Evans 1989;

Huss et al. 2008; white perch Morone americana—Johnson

and Evans 1991; rainbow trout Oncorhynchus mykiss—

Biro et al. 2004b; Atlantic salmon Salmo salar—Finstad

et al. 2004a; roach Rutilis rutilus—Knopf et al. 2007).

Adult individuals have two additional challenges associ-

ated with winter: first, how to acquire and store the

additional energy necessary to produce viable larvae, and

second, how to ensure that the temporal placement of lar-

vae permits them to acquire the maximum benefit from the

summer pulse of food resources. In the following sections,

we discuss constraints on the strategies that are commonly

used to meet all of these challenges. We then go on to

discuss the strategies themselves.

Physiology constrains winter strategies

Fish are ectotherms and hence their ability to interact with

their environment, and acquire energy for growth and

reproduction, strongly depends on temperature. There is an

extensive literature describing how the performance of a

fish changes when it is exposed to different temperatures

(Fry 1971; Elliott 1976; Magnuson et al. 1979; Ohlberger

et al. 2008a; Hasnain et al. 2010). Several metrics (e.g.

preferred temperature, upper and lower lethal tempera-

tures) have been developed to characterize these effects

and all of these metrics are strongly correlated, exhibiting

associations that are similar for both marine and freshwater

species (Fig. 3). These correlations suggest that each fish

species is adapted to perform optimally over a specific

range of temperatures. This is a common property of

ectotherms and its physiological foundation is presented in

several recent reviews (Clarke and Pörtner 2010; Pörtner

2010; Pörtner et al. 2010). This foundation can be

summarized as follows: the species-specific range of tem-

peratures that best supports acquisition of energy from the

environment is bounded by the upper and lower pejus

temperatures; these landmark temperatures define a tem-

perature ‘window’ over which the aerobic scope (the

difference between the highest and lowest rates of aerobic

respiration) is high and relatively constant. The optimal

growth temperature and the preferred temperature are

typically shifted toward the upper end of this window

(Pörtner 2010). The utility of this definition of an ecolog-

ically relevant thermal window (an ERTW) has recently

been confirmed in a study demonstrating that temporal

fluctuations in the abundance of eelpout (Zoarces vivipa-

rous) in the North Sea were strongly linked to changes in

the degree to which environmental temperatures fell within

:wolytisnetnithgiL:hgihytisnetnithgiL

Growth Possible

Prey abundant & visible Prey sparse & invisible

Starvation Likely

Ice PresentIce Absent

Temperature Oxygen

Day

Fig. 2 Schematic illustration ofthe ‘challenge of winter’: the

energy needed to survive winter

food scarcity and successfully

reproduce must be acquired

during the limited period of

summer food abundance

Winter phenology, freshwater fish and climate change 639

123

the ERTW for eel pout (e.g. Pörtner and Knust 2007). Fur-

ther support for this concept can be found in inter-population

studies of freshwater fish based on Magnuson et al. (1979)

simple, empirical definition of the ERTW for a species (i.e.

its ‘fundamental thermal niche’ = the species-specific pre-

ferred temperature ± 2 �C—see Fig. 3). Christie andRegier (1988) used an asymmetric variant of this definition

(i.e. a 4 �C window centred 1 �C below the species-specificpreferred temperature: a definition that should be quantita-

tively similar to the more precise definition proposed by

Pörtner) and found that, for each of four freshwater fish

species (Salvelinus namaycush, Coregonus clupeaformis,

Sander vitreus and Esox lucius) with very different preferred

temperatures (10–24 oC), population productivity increased

with increases in the annual amount of time that water

temperatures fell within the species’ ERTW.

Most freshwater (and marine) fish have a preferred

temperature [4 oC (Fig. 3), yet the maximum temperatureavailable during winter is typically B4 oC. Enzymatic

specialization to a particular temperature range is costly

and broadening that range could compromise performance

in the neighbourhood of the optimal temperature (DeWitt

and Wilson 1998; Pörtner et al. 2006). Hence it is rea-

sonable to suggest that:

• Species with high preferred temperatures will beinefficient energy gatherers under winter conditions

(e.g. warmwater species such as smallmouth bass—

Shuter and Post 1990; Suski and Ridgway 2009a)

• species with low preferred temperatures will be moreefficient energy gatherers under winter conditions (e.g.

coldwater species such as Atlantic salmon—Finstad

et al. 2004b)

• the time and energy needed to re-tool enzyme systemsto improve performance under winter conditions (i.e.

the costs of acclimation) will decrease with decreases in

the difference between preferred and winter tempera-

tures (Pörtner 2006)

Thus, we suggest that the costs of developing physio-

logical strategies to maintain energy acquisition under

winter conditions will be lower for species with lower

preferred temperatures. We also suggest that the impetus

(i.e. the selection pressure) to develop such strategies will

increase with increases in the relative duration of winter

over summer: at low latitudes, where winter duration is

short, the impetus should be weak and it should increase

progressively with the increases in relative winter dura-

tion that accompany increases in latitude (Fig. 1). Also,

increases in winter duration are typically accompanied by

declines in summer surface water temperatures (Shuter

et al. 1983). As a consequence, the annual period of opti-

mal performance for a typical species (i.e. the period when

environmental temperatures fall within its ERTW) should

also change with increases in latitude—its duration short-

ening for warmwater species and extending for coldwater

species (Fig. 4). Therefore, the impetus to develop spe-

cialized adaptations that support energy acquisition during

winter should be strongest in environments that are most

supportive of coldwater species (Fig. 4). This is consistent

with our finding (Table 1) that species with low preferred

temperatures typically feed under winter conditions, and

hence may be considered winter specialists. In contrast,

species with high preferred temperatures are often quies-

cent during winter, thus exhibiting a strategy of tolerating,

rather than exploiting, winter conditions. Energy storage

and husbanding strategies are common to most species that

have been studied (Table 1).

Bioenergetics shape the ecological context for winter

strategies

For organisms living in seasonal environments, an indi-

vidual’s behaviour will respond to seasonal changes in the

abiotic and biotic factors that surround it. Bioenergetics

provide a functional framework, with a standardized

energetic currency, which permits these short and long-

term responses to be rationalized in terms of coherent

-5

35

25

15

5

25155

Preferred temperature (°C)

Crit

ical

ther

mal

met

rics

(°C

)

(iii) Lower Lethal

(ii) OptimalGrowth

(i) UpperLethal

Fig. 3 Thermal performance metrics for freshwater and marine fish.Freshwater species (data from Hasnain et al. 2010): (1) Upper lethaltemperature versus preferred temperature: dashed line = geometricmean regression of upper lethal temp on preferred temperature;

stars = individual species. (2) Optimal growth temperature versuspreferred temperature: solid line = geometric mean regression ofoptimal growth temperature on preferred temperature; closed cir-cles = individual species. Marine species (data from Tsuchida 1995;Pörtner and Peck 2010): the light-shaded region is bounded by therelationships linking upper (i) and lower lethal temperatures (iii) to

preferred temperature. The dark-shaded region illustrates Magnu-son’s definition (preferred temperature ±2 �C) of an ecologicallyrelevant thermal window (ERTW)


123

hypotheses linking physiological, ecological and evolu-

tionary factors (e.g. Kitchell et al. 1977; Jobling 1994;

Hanson et al. 1997). The study of bioenergetics involves

the examination of energy gains and losses, and the transfer

of energy within the whole organism. Ingested energy is

partitioned into the major physiological components lead-

ing to the universal energy budget equation (Jobling 1994):

DE = I � M + P + U + Fð Þ ð1Þ

The energy balance of the fish (DE) is the differencebetween energy ingested as food (I) and the sum of the

energy: (1) expended by metabolic processes (M), (2)

invested in tissue growth (P), (3) lost in the form of

partially oxidized products excreted as urea (U), (4) lost in

faeces (F).

The primary components of this energy budget can be

partitioned into different subunits. The energy costs of

metabolic processes can be partitioned as:

M ¼ Ms þ MSDA þMa þMPL ð2Þ

where Ms is the standard, or basal metabolic rate and

consists of the metabolic costs associated with maintaining

the viability of existing body mass, MSDA (i.e. the specific

dynamic action) includes all the metabolic costs associated

with digesting recently consumed food as well as costs

associated with synthesizing the new tissue required to

support current somatic growth, Ma is the metabolic cost of

maintaining the activity levels typical of life within the

individual’s ecological community, and MPL is the

metabolic cost of maintaining the parasite load carried by

the individual. Total investment in tissue growth (P) can be

partitioned as:

P ¼ Psomatic þ Pstorage þ Pgonads ð3Þ

where Psomatic is energy allocated to somatic or structural

growth, Pstorage is energy allocated to storage products

(typically lipids and glycogen) and Pgonads is energy allo-

cated to reproductive tissue. At each time step in an

individual’s life, available energy must be allocated (Ko-

oijman 2000) among the discretionary components of the

energy budget (e.g. activity, investment in new somatic

tissue, storage products and/or reproductive tissue). The

optimal allocation depends on the energy available, indi-

vidual characteristics (e.g. sex, size, age, stored energy

levels), competition with other individuals and various

environmental characteristics, both biotic and abiotic

(Lester et al. 2004; Shuter et al. 2005). The total metabolic

expenditure is bounded by the aerobic metabolic scope and

hence is continually being reshaped by those aspects of the

abiotic environment (temperature, oxygen levels, pH) that

strongly affect aerobic scope (Pörtner 2010).

The energy available to the individual depends on the

overall intake of energy from foraging, [I - (MSDA ?

F ? U)], offset by the cost of foraging itself (included in

Ma). Both of these elements will vary widely across sys-

tems and species. For a visual feeder, the energy intake

(I) from foraging will vary directly with light intensity (L),

the density of prey resources (R) and the level of foraging

activity. The level of foraging activity itself will depend

on:

(i) temperature (T): the maximum possible foraging rate

will increase with aerobic scope and therefore will

increase with increases in T, peak as T enters and

remains within the ERTW for the species, and then

decline as T increases beyond the species’ ERTW

(Pörtner 2010);

(ii) standard metabolism (Ms): the higher the standard

metabolism, the greater the daily energetic demand

that must be met by foraging; higher demand will

drive higher levels of foraging in order to keep the

probability of death by starvation low (Lima and Dill

1990; Huckstorf et al. 2009);

(iii) metabolic cost of supporting parasite load (MPL):

parasites are not usually lethal to their fish hosts but

they often cause tissue pathology and substantial

Fig. 4 Effect of increasing latitude on: (1) the annual duration ofoptimal performance for two species with different preferred

temperatures (25 and 10 �C). The duration of optimal performanceis the time (% of ice-free season) that lake surface water temperature

remains within the ERTW for the species (Magnuson’s definition:

preferred temperature ± 2 �C); (2) the ratio of ice-free days to icecover days: the impetus to develop specialized strategies for energy

acquisition under winter conditions. The dependence of the lake

surface water temperature regimes on latitude was derived from the

North American FLAKE simulations summarized in Fig. 1


123

Table 1 Species-specific examples of different winter survival strat-egies, grouped by preferred temperature along lines suggested by the

3 thermal guilds of Magnuson et al. (1979): coldwater species with

preferred temperatures \*15 �C; warmwater species with preferredtemperatures [*25 �C; cool water species with intermediate values

Winter survival

strategy

Preferred temperature

\12 12–18 18–24 [24

Energy storage Arctic charr (Finstad et al.2003),

Burbot (Winter storage,Hölker et al. 2004)

Atlantic salmon (Berg et al.2010;

Finstad et al. 2010), Rainbowtrout (Biro et al. 2004b;Post and Parkinson 2001)

Striped bass(Hurst and

Conover 2003;

Hurst et al. 2000),

European perch(Huss et al.

2008),

European perch(Heermann et al.

2009),

Gizzard shad(Ultsch 1989)

Atlantic silverside (Schultz and Conover1997),

Mosquito fish (Reznick and Braun 1987),

Smallmouth bass (Mackereth et al. 1999),

Roach (van Dijk et al. 2005)

Active:

Feeding ? risk

avoidance

Arctic charr (Finstad et al.2003),

Coregonus fontanae,Corgonus albula (Hellandet al. 2007),

Lake trout (Blanchfield et al.2009), Brown trout(Amundsen and Knudsen

2009)

Whitefish (Siikavuopio et al.2010),

Atlantic salmon (Cunjak1996; Finstad et al. 2010,

2004a, b; Linnansaari et al.

2008),

Brook trout (Cunjak andPower 1986)

Pike (Kobler et al.2008a),

White crappie(Tschantz et al.

2002)

White bass (Cooke et al. 2003), Roach(Brönmark et al. 2008)

Active-

Quiescent

Ruffe (Hölker and Thiel 1998) Yellow perch(Johnson and

Evans 1991;

Ultsch 1989),

Black crappie(Cooke et al.

2003; Tschantz

et al. 2002)

Green sunfish (Kolok 1991; Tschantz et al.2002),

Bluegill (Shoup and Wahl 2011; Tschantzet al. 2002; Ultsch 1989),

Pikeperch (Kirjasniemi and Valtonen1997; Lappalainen and Vinni 2001;

Vehanen and Lahti 2003; Teletchea

et al. 2009),

Roach (van Dijk et al. 2005; Hölker andBreckling 2005; Binner et al. 2008),

Bream (Hölker 2006)

Quiescent Burbot (summerquiescence-(Hardewig

et al. 2004; Finstad et al.

2010)

Blacknose dace(Ultsch 1989)

Smallmouth bass (Shuter et al. 1989; Kolok1991; Barthel et al. 2008; Suski and

Ridgway 2009b),

Largemouth bass (Lemons and Crawshaw1985; Hanson et al. 2008; Tschantz et al.

2002; Hasler et al. 2009a, b),

Pumpkinseed (Evans 1984),

Carp (Ultsch 1989),

Brown bullhead (Lemons and Crawshaw1985; Ultsch 1989)

Storage strategists allocate energy to storage products (e.g. lipids) toward the end of their high productivity season (summer-fall for all species

except the extreme winter specialist, burbot). Active strategists balance active feeding with facultative behaviours that limit both predation risk

and avoidable energy drains. Quiescent strategists remain in sheltered habitats, exhibit minimal movements, do not actively feed and may exhibit

anticipatory physiological changes that increase their fitness for a sedentary winter existence. Active-quiescent strategists exhibit some aspects of

both strategies. Preferred temperatures for most species were obtained from (Hasnain et al. 2010). Sources for other species are: Arctic char(Mortensen et al. 2007), Atlantic silverside (Conover and Present 1990), Burbot (Binner et al. 2008; Hofmann and Fischer 2002), Coregonusfontanae, C. albula (Ohlberger et al. 2008a), European perch (Hokanson 1977), Mosquito fish (Condon et al. 2010), Pikeperch (Wang et al.2009), Roach (van Dijk et al. 2002), Striped bass (Coutant 1990)


123

metabolic stress, thus imposing an additional meta-

bolic cost on the host (Lemly and Esch 1984; Knopf

et al. 2007; Seppanen et al. 2008); MPL increases

with parasite load and consequently increases the

obligate daily energetic demand (Ms ? MPL); higher

demand will drive higher levels of foraging in order

to keep the probability of death by starvation low;

(iv) prey resources (R): as prey density increases, the

level of foraging activity will begin to decline, since

increases in density will lead to increases in the

proportion of each feeding period that the individual

spends digesting food, as well as decreases in the net

energy the individual will gain for each unit of

energy expended on foraging (Holling 1959);

(v) predation risk (PR): increases in predation risk (e.g. from

increased predator density) are typically accompanied

by a decline in the optimal level of foraging activity,

since lower foraging activity typically decreases expo-

sure to predation and hence offsets increases in predation

risk (Biro et al. 2004a; Chiba et al. 2007);

Therefore, the energy intake rate (I) will depend on L, T,

(Ms ? MPL), R and PR. Now, if [Ma] is larger or smaller

(i.e. =) than [I - (MSDA ? F ? U)], the activity costsassociated with foraging will be greater, or less, than the

energy that foraging provides. These bioenergetic

inequalities shape the ways in which ecological factors (L,

T, PL, R, PR) drive the cost-benefit tradeoff that deter-

mines the realized level of winter foraging activity.

During winter, negative energy budgets are common and

risk of starvation mortality is high because:

(i) negligible rates of primary production under low

light and temperature conditions lead to low prey

densities;

(ii) the net energy gain from active, visual foraging is

often negative because of the longer search times,

and consequently higher activity costs, required to

successfully capture prey when both light levels and

prey densities are low;

(iii) the overall benefit from active foraging may be

reduced due to increased predation risk from preda-

tors that are adapted to low temperature conditions

(e.g. endotherms, cold-adapted ectotherms);

(iv) temperatures may reach levels low enough to evoke

physiological inhibition of foraging activity.

The expected lifetime for a fish with a negative energy

budget depends on the overall rate of energy depletion, the

initial level of pre-winter energy storage (Einitial), and the

critical minimum storage level needed for survival (Ecrit).

The rate of energy depletion is set by the difference

between metabolic costs and energy intake. Death ensues

when energy levels fall to Ecrit (Fig. 5).

Dealing with winter: strategies for survival

and reproduction

Strategies for dealing with winter reductions in light,

temperature and prey resources fall into three broad cate-

gories: toleration, specialization, and reproduction. The

first two deal with individual survival over winter, while

the latter deals with offspring survival. Figure 5 illustrates

two different strategies for managing activity to increase

winter survival, given a fixed level of stored energy in fall.

If conditions are such that the energy depletion rate under

optimal foraging provides no net gain in energy (Ma C

[I - (MSDA ? F ? U)]), then, at best, the energy depletion

rate will equal the rate associated with no foraging

(Ms ? MPL) and the animal will receive no benefit from its

exposure to the level of predation risk associated with

foraging. In this situation, the best winter survival strategy

will always be to cease foraging, thus reducing both met-

abolic costs and predation risk. This is one aspect of a

toleration survival strategy. Conversely, if the optimal

foraging rate can sustain a net energy gain to the organism

(Ma \ [I - (MSDA ? F ? U)]), then the storage depletion

Time

EcritSto

red

en

erg

y

T*surv

Inet = I – (Msda + F + U)

Einitial

Toleration strategy optimal:foraging provides no benefit

Specialization strategy optimal:foraging beneficial

Ma = Inet

Ma > Inet Ma < Inet

Fig. 5 Schematic illustrating how the usefulness of active feedingunder winter conditions is determined by: (1) the pre-winter level of

stored energy (Einitial) and the minimum level required to maintain

viability (Ecrit); (2) the ingestion rate (I) and the energetic losses

associated with that ingestion rate (Ma, MSDA, F, U); (3) the obligate

energy demand (Ms ? MPL). These factors determine the expected

lifetime (Tsurv) under winter conditions. In the absence of feeding, the

expected lifetime (T*surv) is determined jointly by the energy storage

levels and the obligate energy demand: T*surv = (Einitial-Ecrit)/

(Ms ? MPL). In situations where the energetic cost of active foraging

(Ma) is [the net energy gained from foraging (Inet), then foragingprovides no benefit: use of stored energy is[(Ms ? MPL) and Tsurv is\T*surv. In such situations, the optimal strategy is to cease feedingand adopt a toleration strategy. In situations where foraging is

beneficial (Ma \ Inet), then the optimal strategy is to engage in winterforaging as part of a specialization strategy. The optimal foraging rate

would be subject to the degree of predation risk—if an increase in

predation risk causes a drop in expected lifetime, then the animal

should reduce foraging activity so as to reduce its exposure to this

increased risk


123

rate will be reduced and the expected lifetime (Tsurv,

Fig. 5) will be extended. Under these conditions, the

optimal winter survival strategy will be to forage at a rate

that provides the optimal trade off between the mortality

risks from starvation and predation (Bull et al. 1996). This

is a specialization survival strategy.

Toleration strategies include both the pre-winter storage

of energy for winter use (Berg et al. 2009; Hurst and Co-

nover 2003) and the minimization of demands on that stored

energy during winter (Evans 1984; Shuter et al. 1989).

Specialization strategies focus on continuing energy

acquisition during winter (Hölker et al. 2004; Finstad et al.

2010). Reproductive strategies focus on timing reproduc-

tion to ensure effective access by larvae to the summer

production pulse (Yeates-Burghart et al. 2009; Migaud et al.

2010; Pörtner and Peck 2010). Toleration and specialization

strategies are of particular importance for juvenile fish since

they typically experience higher winter mortality risk

because of their higher mass specific metabolic rates and

lower lipid storage capacities (Ultsch 1989; Shuter and Post

1990). Reproductive strategies are the province of mature

adults and are designed to maximize offspring survival,

potentially at the expense of parental survival.

Toleration survival strategies

There are two common toleration strategies: energy storage

prior to winter and minimization of energy usage during

winter.

Energy storage is a widespread adaptation to seasonality

(e.g. Schultz and Conover 1997; Finstad et al. 2010).

Energy reserves are typically acquired in times of abundant

food supply or where physical conditions support adequate

physiological performance of the individual (Hurst 2007).

Fish commonly store energy reserves in the form of non-

polar lipids (Jobling 1994) and for temperate freshwater

fishes, this usually takes place during summer and fall (e.g.

Hurst and Conover 2003). There are many studies docu-

menting accumulation of energy storage products in

juvenile fish (van Dijk et al. 2005), and similar behaviour

has been documented in a few studies of adults (Dawson

and Grimm 1980; Adams et al. 1982; Encina and Granado-

Lorencio 1997). Lipids and glycogen are usually the first

reserves to be mobilized when food becomes scarce (Shi-

meno et al. 1990; Sargent et al. 2002; Hölker and Breckling

2005). However, with extended periods of starvation, these

reserves will become depleted and then liver and muscle

protein will be mobilized to support metabolism (Love

1974; Shimeno et al. 1990). A variant of this storage

strategy, found among adult females of spring spawning

species, is the winter utilization for maintenance metabo-

lism of ovarian energy, originally allocated to egg

development (Henderson et al. 1996, 2000).

Facultative and obligate controls on winter energy usage

have been observed in many fish species. Obligate reduc-

tions in basal metabolism, cued by the reductions in

photoperiod that precede winter, have been identified in

several temperate freshwater fish species (Beamish 1964;

Evans 1984). Facultative behaviour that serves to minimize

activity metabolism during winter is also common. This

typically involves selection of microhabitats (e.g. boulders,

groundwater inflows, deeper areas in the water column)

with reduced exposure to high and/or variable water cur-

rents. Many studies of river and lake systems have reported

such behaviours. The winter use of sheltered areas (e.g.

deep water areas, pools, side channnels) has been observed

for cyprinids (Heermann and Borderding 2006; Irmler et al.

2008; Rakowitz et al. 2009), salmonids (Cunjak and Power

1986; Swales et al. 1986) and a variety of other species

(e.g. Esox lucius Kobler et al. 2008b). Studies of brook

trout Salvelinus fontinalis (Cunjak and Power 1986) con-

cluded that typical over-wintering behaviour was

consistent with a strategy of choosing habitats to minimize

energy costs. All of these diverse examples of winter

habitat selection can be interpreted as vehicles for reducing

both swimming cost and predation risk.

States of extreme inactivity during winter have been

observed in a variety of fish species. Animals in such a

quiescent state typically remain in sheltered habitats,

exhibit minimal movements and do not feed (Lemons and

Crawshaw 1985; Shuter et al. 1989). However, they may

remain active in the absence of sheltering habitats (Shuter

et al. 1989) and still respond to direct stimuli—they do not

exhibit the obligate entry into a deep torpid state that is

typical of hibernating ectotherms such as turtles and lizards

(Ultsch 1989). Comparative studies of the physiology of

quiescent-winter species and active-winter species have

found that quiescent species:

(i) do not exhibit the hypertrophy of heart and liver

typical of winter acclimation in active species

(Tschantz et al. 2002);

(ii) have a smaller scope for cardiac output than active

species (Cooke et al. 2003);

(iii) exhibit a significantly larger drop in basal metabolic

rate and spontaneous activity under winter conditions

than is expected, given the temperature difference

between summer and winter (Lemons and Crawshaw

1985; Tschantz et al. 2002); this drop may reflect

anticipatory reductions in basal metabolic rate trig-

gered by declining photoperiod (Evans 1984).

Specialization survival strategies

Fish can adapt their behaviour and physiology to increase

their success during stressful periods, and some species are


123

better adapted to winter stresses than others. Species that

perform well during winter may be regarded as ‘‘winter

specialists’’. Following the bioenergetic framework

described above, winter ‘specialists’ are those species that

are proficient at both capturing prey under winter condi-

tions and converting captured prey biomass to useable

energy. This is achieved through adaptations to low light,

low prey abundance, low temperatures and, in some sys-

tems, low oxygen levels.

Fish living at high latitudes with severe winters and

short days seem capable of detecting very low light levels.

For example, studies of several species in both Norway

(Strand et al. 2008) and Finland (Jurvelius and Marjomaki

2008) have shown that diel behaviour patterns driven by

day-night cycling continue unimpeded in waters covered

by thick layers of ice and snow. Successful feeding in

reduced light can be achieved by improving vision or by

employing other senses that do not depend on light (e.g.

mechano-reception or chemoreception—Janssen and

Corcoran 1993; Liang et al. 1998). In lakes with long ice-

cover and deep snow cover, species that are less dependent

on light for feeding will have a competitive advantage over

visual feeders. However, for many fish, the effect of

ambient light on capture success is probably less critical

than the low resource biomass found in such lakes because

of their low levels of primary production.

Some salmonids benefit from ice-cover and have poorer

performance during ice-free winter periods (Finstad et al.

2004c; Helland et al. 2011). This is probably related to

increased predation risk in ice-free conditions, causing

individuals to reduce their foraging times. Another factor is

metabolism, which is reduced in darkness under ice-cover

but remains high in the absence of ice due to heightened

activity. The result is a net loss of energy because food

levels are too low to permit the increases in consumption

needed to maintain the heightened activity. Arctic charr are

found at higher latitudes than any other freshwater fish

species and are therefore the species most likely to exhibit

specific adaptations for surviving under conditions where

winters are long and productivity is low. Laboratory studies

of charr have found them capable of growing at very low

temperatures (*2-5 �C : Larsson et al. 2005) while fieldand laboratory studies have shown that they feed throughout

long periods of ice-cover (Klemetsen et al. 2003; Svenning

and Klemetsen 2007; Amundsen and Knudsen 2009) and

can exhibit over-winter growth (Siikavuopio et al. 2010).

Size classes that have grown large enough to switch their

diet from zooplankton to benthic invertebrates may feed

better over winter since winter abundance of benthic

invertebrates can be much greater than zooplankton abun-

dance (Byström et al. 2006; Hölker 2006).

To benefit from feeding at low prey densities, a high

food conversion efficiency is required and arctic charr have

a growth efficiency (per unit of food) that is almost twice

that of brown trout (Salmo trutta), a closely related species

with similar thermal performance parameters and food

preferences (Finstad et al. 2011; Helland et al. 2011).

These potentially competing coldwater species coexist in

many lakes across northern Europe. Their ability to coexist

may be founded on species-specific sets of contrasting

seasonal adaptations that translate into a pattern of reci-

procal competitive advantage—the aggressive, energy

demanding behaviour of brown trout giving it a competi-

tive advantage over arctic charr during the summer period

of prey abundance, while the superior winter feeding

abilities and conversion efficiencies of arctic charr make it

the superior competitor during winter when prey are rare

(Finstad et al. 2011).

Some species are strictly cold-adapted and stay in cold

lake habitats at all times of the year. One example of an

extremely cold-adapted fish is Coregonus fontanae, a

species endemic to Lake Stechlin in northern Germany and

closely related to the more common European vendace (C.

albula). Coregonus fontanae has a preferred temperature of

4.2 �C and its swimming performance is optimal at about4 �C (Ohlberger et al. 2008a, b). It remains in deep watersthroughout the year and hence always experiences winter-

like temperatures of 4–6 �C (Mehner et al. 2010). Anotherexample of an extreme winter specialist is burbot (Lota

lota), a species that is most active in winter and exhibits

little movement in summer (Hölker et al. 2004). At higher

summer temperatures, its feeding and basal metabolic rates

are reduced, it seeks physical shelter and its energy stores

are depleted (Binner et al. 2008; Nagel et al. 2011). During

winter, it is an efficient benthivorous and piscivorous

predator (Lehtonen 1998) and its energy stores are refilled

(Binner et al. 2008; Nagel et al. 2011). It may be advan-

tageous for burbot to exhibit this unusual strategy of high

hunting and feeding activity during winter because most of

its potential competitors are relatively inactive and hence

burbot would experience reduced interspecific food com-

petition and lower predation risk (Hölker et al. 2004).

Reproductive strategies

Many temperate freshwater fish species have a single

spawning period annually (Scott and Crossman 1973), and

that period is typically placed at either the start (fall

spawners) or the end (spring spawners) of winter. For many

North American freshwater fish, the timing of spawning is

directly linked to thermal performance: fish with low pre-

ferred temperatures (coldwater fish) spawn in the fall and

fish with higher preferred temperatures (cool/warmwater

fish) spawn in the spring (Fig. 6). Timing is regulated by a

cuing system based on photoperiod and temperature, such

that spawning can only occur within a time window (spring


123

or fall) defined by photoperiod, but the exact date within

this window is determined by the date when water tem-

peratures exceed a species-specific spawning temperature

(Bradshaw and Holzapfel 2007). Given a broad time win-

dow and a fixed spawning temperature, the spawning date

for a widely distributed spring spawner should vary directly

with latitude and this has been observed for several Euro-

pean species (Lappalainen and Tarkan 2007). Among

North American freshwater fish, the spawning temperature

itself is typically *5 �C less than the preferred tempera-ture for both spring and fall spawners (Fig. 6). This pattern

can be rationalized as follows:

(i) the timing of spawning should be adjusted to permit

larvae to maximize the benefit they can gain from the

annual summer production pulse;

(ii) performance of coldwater fish typically exceeds that

of warmwater fish during the low temperatures that

precede and follow the annual production peak;

hence fall spawning, with consequent slow embryo

development under winter temperatures, permits the

larvae of coldwater fish to hatch and begin feeding at

the start of the production pulse when low temper-

atures maximize their efficiency at using the food

available; in addition, by positioning the spawning

temperature somewhat below the preferred temperature,

adults are able to utilize all of the fall feeding period to

gather energy for expenditure on reproduction;

(iii) performance of warmwater fish typically exceeds that

of coldwater fish during the period of warmer

temperatures that hold during much of the production

pulse; therefore, spring spawning, at a temperature

somewhat below the preferred temperature, permits

rapid embryo development during spring/early sum-

mer so that larvae can begin feeding during periods

when both their feeding efficiency and food avail-

ability is high; in addition, this affords adults the

opportunity of ‘assessing’ the severity of winter as it

proceeds and ‘deciding’ whether to skip spawning

and use the energy stored in reproductive products for

self maintenance (Henderson et al. 1996).

This linkage between thermal performance and the

timing of spawning leads to temporal partitioning of the

food resources available to young-of-year fish during the

annual production pulse. Such partitioning limits compe-

tition among species that differ widely in thermal

performance and thus supports the wide diversity in ther-

mal performance typical of the fish communities found in

deeper temperate zone lakes.

Fig. 6 Phenology ofreproduction for fall and spring

spawning fish. Each box plotgives the optimal spawning, egg

development and growth

temperatures for these two

reproductive classes of fish. The

solid-shaded regions mark thetwo periods in a year when

surface water temperatures lie

within the ERTW of the fall

spawner. The hatched-shadedregion marks the single periodin a year when surface water

temperatures lie within the

ERTW of the spring spawner.

The data summarized in the boxplots are from a compilation ofthermal performance metrics for

Canadian freshwater fish

species (Hasnain et al. 2010).

Units for all box plots are �C


123

Inter- and intra-specific variation in winter strategies

Most species exhibit some form of energy storage strategy

(Table 1). Even extreme winter specialists such as burbot

utilize this strategy, with winter replacing summer as the

season of storage accumulation (Hölker et al. 2004; Nagel

et al. 2011). However, inter-specific variation in other

winter strategies is extensive and, as expected, exhibits

strong links with thermal performance: there is an

increasing emphasis on quiescent strategies among species

with higher preferred temperatures (Table 1) and the sea-

sonal timing of spawning is strongly linked to thermal

performance (Fig. 6). These associations are not rigid—

some euryoecious species can deploy variants of several

strategies. For example, roach will engage in winter

migrations between lake and river environments, balancing

growth opportunities against predation risk (Brönmark

et al. 2008) but, when migration is impossible, they will

adopt an opportunistic-quiescent strategy with respect to

foraging: they will abandon active foraging but will

opportunistically feed on prey that enter their refuge hab-

itats (Hölker and Breckling 2005). Similarly, smallmouth

bass will elect a quiescent strategy in the presence of refuge

habitats but will adopt active predator avoidance behaviour

(i.e. schooling) in their absence (Shuter et al. 1989).

With respect to reproductive strategies, there are

exceptions to the link between thermal performance and

spawning timing, but they are not inconsistent with the

rationale outlined above. For example, spring spawning

morphs of arctic charr exist in both England and Norway

(Frost 1965; Klemetsen et al. 1997). However, these are

deep profundal morphs experiencing more or less constant

temperatures of 4 �C, year-round and in the English pop-ulation, they represent only a very small proportion

(*4 %) of the adults (Baroudy and Elliot 1994). There arealso some exceptional populations within the Coregonus

albula complex. Fall spawning is typical for most popu-

lations, but some populations spawn in winter or spring

(Vuorinen et al. 1981; Mehner et al. 2010, 2012). These

populations appear to have diverged from ancestral fall

spawners, in response to intense selection pressure imposed

on zygotes and juveniles by adverse winter oxygen con-

ditions (Vuorinen et al. 1981).

For species with broad geographic distributions, con-

siderable intra-specific variation in winter strategies is

expected. As the level of winter stress increases along the

climatic gradient found within a species’ range, selective

pressures should act to strengthen its elected winter sur-

vival strategies. Trends of this sort have been noted in

marine species (Conover et al. 2005) and might be

expected to be stronger in freshwater limnetic species,

where the constraints on gene flow imposed by watershed

isolation should favour local adaptation. Indeed, examples

of local adaptation in both storage and reproductive strat-

egies are evident in the recent literature (Yeates-Burghart

et al. 2009; Finstad et al. 2010; Berg et al. 2011). However,

there are limits to the effectiveness of some strategies. For

example, a pure toleration strategy, consisting of energy

storage and winter quiescence, must become increasingly

ineffective with the joint increases in winter length and

decreases in summer production that accompany increases

in latitude. Thus winter may play a significant role in

shaping the zoogeographic boundaries of some species.

Winter strategies overwhelmed: the location

of zoogeographic boundaries

The northern zoogeographic boundaries of some species

may be shaped by the presence of winter conditions severe

enough to overwhelm the strategies available for coping

with them. Shuter and Post (1990) showed that the current

positions of the northern zoogeographic boundaries for

smallmouth bass and yellow perch in North America could

be explained directly in terms of how their phenologies of

reproduction, growth and winter energy usage depend on

the phenology of winter. They also listed several other

species that might be similarly affected. Studies of some

marine species suggest that similar considerations may be

shaping their northern distributional boundaries (Conover

and Present 1990; Pörtner and Peck 2010). Since both the

costs of coping with winter (Figs. 2 and 3) and the strate-

gies for dealing with it (Table 1; Fig. 6) are linked to

thermal performance, we might expect to find a relatively

simple link between measures of thermal performance and

the position of distributional boundaries. Shuter et al.

(2002) showed that, for a large subset of North American

fish, species with higher preferred temperatures exhibited

northern distributional boundaries that were associated

with warmer longer summers and shorter winters. We

extended the analyses of these data to ask the more specific

question of whether the positions of these northern distri-

butional boundaries were associated with the fraction of the

ice-free period when surface water temperatures were

within the ERTW of each species (Fig. 7). We found that

these northern distributional boundaries were located

where annual water temperature regimes provided minimal

exposure to temperatures that lie within species-specific

ERTW’s.

An interesting corollary to this analysis is that, for

southern lakes, a significant portion of the ice-free period

exhibits surface temperatures that are optimal for cold-

adapted fish (Fig. 7). These temperatures are found in the

‘shoulder’ seasons of spring and fall and they are sufficient

to support viable populations of these species provided

that:


123

(i) the lake stratifies in summer, does not exhibit hypolim-

netic oxygen depletion during stratification and thus

provides a coldwater summer refuge to sustain the

population (Evans 2007; Blanchfield et al. 2009);

(ii) the lake does not stratify, but surface temperatures do

not reach lethal levels and the fish is free of

competitors with higher preferred temperatures

(Gunn 2002; Mackenzie-Grieve and Post 2006).

The relationships between thermal metrics and bound-

aries (Fig. 7) are relatively loose, with much unexplained

variation. This variation likely reflects the influence of a

broad range of abiotic and biotic factors that modify the

influence of climatic conditions on the aquatic environ-

ment. For example, systematic differences in lake size and

morphometry can generate systematic differences in both

ice phenology and summer water temperatures despite

common climatic conditions. These sorts of interactions

among driving variables likely generate the ‘fuzzy’ edges

that characterize the zoogeographic boundaries for many

freshwater fish species (e.g. Shuter et al. 1980).

Another important abiotic factor is winter oxygen

availability, which varies with both lake morphometry and

winter duration. In shallow eutrophic lakes, long winters

can lead to mass mortalities of fish and other biota (i.e.

winter-kill events) due to severe oxygen depletion in late

winter. Such events are caused (Greenbank 1945) by: (1)

ice cover stopping inputs of atmospheric oxygen to the

lake; (2) ice, and especially snow cover, cutting off light

and thus stopping oxygen inputs from photosynthesis; (3)

consumption of available oxygen, particularly near the lake

bottom, by biological degradation of organic matter. The

degree of oxygen depletion will vary directly with increa-

ses in summer productivity, length of ice cover and benthic

water temperature, and inversely with increases in lake

depth and the ratio of lake volume to benthic-surface-area

(Fang and Stefan 2000; Meding and Jackson 2001; Clilverd

et al. 2009; Liboriussen et al. 2011). Mortality among

resident biota will be augmented by additional by-products

of biological degradation, such as toxic gases (hydrogen

sulphide, methane) and carbon dioxide, and can be exac-

erbated by biological factors such as fungal (Bly et al.

1993) and bacterial infection (Hayman et al. 1992), stress

(O’Connor et al. 2010), parasite load and age (Kennedy

et al. 2001). Winter-kill is a common phenomenon among

shallow lakes in regions characterized by long winters (e.g.

Alaska—Clilverd et al. 2009; Alberta—Danylchuk and

Tonn 2003; Eaton et al. 2005; Danylchuk and Tonn 2006;

Finland—Ruuhijarvi et al. 2010). Greenbank (1945) esti-

mated the annual risk of occurrence for a lake typical of the

Michigan lakes he studied to be *0.33 year-1 whileMagnuson et al. (1998) estimated the risk for individual

Wisconsin lakes to range from 0.05 to 0.2 year-1. In

central Europe, the risk is much lower (e.g. Geiger 1962

reported no winter kills in Switzerland over a 10 year

period). However, the impact of even a single winter kill

event can have long lasting effects on the lake that expe-

riences it (e.g. Ridgway et al. 1990; Eaton et al. 2005).

Lakes that are subject to frequent winter kill events

typically support a unique community of fish species that

possess a range of specialized behavioural and physiolog-

ical strategies for tolerating winter oxygen deficits (Tonn

et al. 1990). Where winters are very long and low oxygen

levels are common and persistent, toleration strategies fail

and fishless lakes become common (Jackson et al. 2007). In

such lakes, the zooplankton and phytoplankton communi-

ties, and the annual pattern of nutrient cycling, differ

widely from what is common in lakes that support fish

communities (Jackson et al. 2007; Balayla et al. 2010;

Jeppesen et al. 2010).

Latitude

25°C

20°C15°C

10°C

40

30

20

10

0

30

20

10

40 50 60 70

Pre

ferr

ed

tem

per

atu

re

Du

rati

on

op

tim

al

per

form

ance

(% ic

e fr

ee s

easo

n)

12.5 4.5 -3.4 -11 Mean annualair temperature (°C)

Latitude/Climate at boundary

A

B

25°C

15°C

20°C

Fig. 7 a For North America: the association between increasinglatitude and the annual duration of optimal performance for species

with preferred temperatures of 25, 20, 15 and 10 �C. The duration ofoptimal performance is the time (% of ice-free season) lake surface

water temperatures remain within the ecologically relevant thermal

window for the species (Magnuson’s definition: preferred

temp ± 2 �C). Lake surface water temperatures were generated fromthe FLAKE simulations for North America illustrated in Fig. 1; mean

annual air temperature at each latitude is consistent with the FLAKE

simulations. b Preferred temperatures for 23 North American fishspecies plotted against the latitude marking the northern zoogeo-

graphic boundary for each species (see Shuter et al. 2002 for details).

Block arrows illustrate the fact that, for each temperature preferenceclass, the typical latitude marking the northern zoogeographical

boundary for species belonging to the class corresponds to the latitude

at which duration of optimal performance for the class falls to zero.

The striped bar marks the range of latitudes that separate thecontinental land mass from the Arctic Ocean


123

Winter strategies for tolerating oxygen deficits:

species endemic to winter-kill lakes

The survival strategies that permit food acquisition under

winter conditions are paralleled by the specialized oxygen

deficit strategies of the fish species that persist in winter-

kill lakes. In Wisconsin, winter-kill lakes are characterized

by a unique community of fish species (Klinger et al. 1982;

Magnuson et al. 1985) that exhibit a range of simple

adaptations for tolerating low oxygen conditions: migration

to high-oxygen micro-refuges, orientation to higher oxygen

concentrations at the ice-water interface and morphological

adaptations that permit the direct breathing of air trapped in

bubbles at the ice-water interface. In Finland, the crucian

carp (Carassius carassius L.) is often the only fish species

found in lakes that are susceptible to winter-kill. This

species has adapted to life in low oxygen conditions by

developing an efficient anaerobic respiratory system

(Holopainen et al. 1986; Nilsson and Renshaw 2004).

Such oxygen deficit specialists are often the only species

that can persist in lakes that are subject to frequent winter-

kill events. These same species are rare or absent in lakes

that do not suffer from winter-kill events. It seems likely

that this presence/absence pattern stems from the fact that

the costs and inefficiencies associated with winter oxygen

deficit strategies become a sufficient burden in more benign

environments to prevent successful competition with the

wide range of species that can live in those benign

environments.

Sensitivity to climate change is shaped by winter

strategies

Historical trends in the climate of the Northern Hemisphere

have been accompanied by significant changes in the

phenology of ice cover in both lakes and rivers (North

America: Magnuson et al. 2000; Lemke et al. 2007; Benson

et al. 2012. Europe: Livingstone 1997; Stonevicius et al.

2008; Weyhenmeyer et al. 2008. Asia: Smith 2000; Batima

et al. 2004; Vuglinski 2006). Current trends (e.g. Trenberth

et al. 2007) and future projections (e.g. Christensen et al.

2007) suggest that, over the next century, winter duration

will decrease progressively and winter phenology will shift

in concert with that decrease. These changes will be

accompanied by increases in summer surface water tem-

peratures and shifts in the thermocline depth of lakes.

Significant changes in both lake water levels and river flow

rates are also likely, with the direction of change (increase

or decrease) depending as much on climatic region (e.g.

maritime vs mid-continent) as on absolute change in air

temperature. The freshwater ecosystems resident in these

water bodies share a wide range of characteristics that

make them vulnerable to the impacts of climate change

(Woodward et al. 2010). The vulnerability of these eco-

systems is accentuated by the fact that they are populated

by fish species whose behavioural and physiological

strategies have been shaped by the need to deal with

adverse winter conditions. The responses of these strategies

to the rapid relaxation of the adversities that shaped them

will play a significant role in the overall impact of climate

change on these ecosystems.

Decreases in the duration of ice cover will progressively

reduce the competitive advantage that winter specialists

have over eurythermal species (Pörtner 2006), promoting

both decreases in their local abundance and contractions of

their distributional ranges (e.g. Finstad et al. 2011; Helland

et al. 2011; Ulvan et al. 2012). This will be exacerbated by

the difficulties that winter specialists will face in dealing

with the epilimnetic summer warming that will accompany

shorter winters (Pörtner 2006; Somero 2010). Rapid

warming may overwhelm the ability of such organisms to

effectively adapt to these changes, although recent work

(Salinas and Munch 2012) suggests that some fish species

have adaptive mechanisms (e.g. transgenerational plasticity

of optimal growth temperature) that can operate on quite

short time scales. The potential impact that the disappear-

ance of winter may have on winter specialists generally is

most clearly seen in the disjunct distributions of species

adapted to persist in winter-kill systems—these winter

specialists are rare or absent in those systems that are free

of winter-kill (Tonn et al. 1990; Magnuson et al. 1998).

Attempts to forecast how climate change might re-shape

the distributional boundaries of freshwater fish in the

Northern Hemisphere began in the 1980’s (e.g. Meisner

et al. 1987; Shuter and Post 1990; Shuter and Meisner

1992) and are continuing (e.g. Sharma et al. 2007). These

studies consistently predict that the northern boundaries for

warmwater (e.g. smallmouth bass Micropterus dolomieu)

and coolwater fish (e.g. yellow perch Perca flavescencs and

European perch Perca fluviatilis) will extend northward

over the period 2000–2100. In contrast, coldwater species

are expected to undergo habitat reductions (e.g. Salvinus

Alpinus—Gerdeaux 2011; Salvelinus namaycush—Gunn

et al. 2004; Salvelinus fontinalis—Meisner 1990; Coreg-

onus artedi—Sharma et al. 2011) along the southern

boundaries of their zoogeographic distributions. In the

deeper lakes along these southern boundaries, cold hypo-

limnetic waters provide summer refuges for coldwater

species. Extensions of the stratification period in some of

these lakes (particularly eutrophic lakes) will lead to severe

and pervasive hypolimnetic oxygen deficits in late summer.

This will reduce/eliminate such refuges, leading to reduc-

tions in abundance of the local populations that rely on

them (Stefan et al. 2001; Plumb and Blanchfield 2009) and

ultimately to contractions in the zoogeographic ranges of


123

these species. Most of this work has focused on North

American distributions; however, a recent empirical study

of the occurrence and relative density of Eurasian diadro-

mous species found that approximately 20 % of the species

examined were sensitive to changes in winter conditions

(Lassalle and Rochard 2009).

If changes in winter phenology promote range exten-

sions for both cool and warmwater fish, then fish species

richness should increase in many parts of the north tem-

perate zone (e.g. Meisner et al. 1987). Recent studies of

distributional changes in French rivers are consistent with

such predictions: in most locations, fish species richness

increased, warm-water fish species new to the area were

observed and most native species exhibited habitat

expansions (Daufresne and Boet 2007). Trends toward

increased richness may be blocked or reversed in those

locations where changes in climate are accompanied by

changes in the frequency and severity of winter floods

(Trenberth et al. 2007). Given the extensive use of river

habitats by limnetic fish populations for spawning sites,

nursery areas and winter refuges, any systematic change in

the frequency and/or intensity of winter floods could have

significant impacts on populations of these species, as well

as on populations of riverine fish. For example, Doll and

Zhang (2010) predicted a decrease in fish species richness

in those rivers where discharge rates will decrease due to

climate change. Such decreases are predicted for only a

few rivers, but some of these are located in biogeograph-

ically valuable regions (e.g. the Amazon basin).

Changes in species richness can cause many other eco-

logical effects. Perhaps the most extreme effects forecast in

the literature involve those associated with the relaxation of

winter kill conditions in shallow fertile lakes. Together

with the expected shifts in zoogeographic boundaries, this

will open up new habitats for colonization by fish and other

long lived aquatic vertebrates over broad geographic areas,

leading to shifts in nutrient cycles, changes in the seasonal

cycling of phytoplankton and zooplankton biomass and

changes in water quality that are typically associated with

eutrophy (e.g. increased turbidity, higher chlorophyll lev-

els, increased prevalence of cyanophyta, Jackson et al.

2007; Balayla et al. 2010; Jeppesen et al. 2010; Sorensen

et al. 2011). At higher trophic levels, initial increases in

richness will promote changes in predation and competi-

tion pressures that can strongly affect final community

composition. Sharma et al. (2007) argued that increased

predation by invading smallmouth bass would pose a

serious threat to native cyprinid species (as per Jackson

2002), while Ng and Gray (2011) argued that climate dri-

ven shifts in predator–prey relationships could cause

increased bioaccumulation of persistent chemicals in

freshwater food chains. Buisson and Grenouillet’s (2009)

study of climate change impacts on French rivers suggested

that species diversity would increase more than trait

diversity in many locations, leading to increases in the

overall intensity of competition for resources (e.g. food—

Vander Zanden et al. 1999). Such shifts could, for example,

cause increased hybridisation rates due to increased com-

petition for spawning sites resulting from greater overlap in

species-specific spawning times.

In addition to changing limnetic and riverine fish habi-

tat, changes in winter phenology will also lead to changes

in the phenology of fish life cycles. Such changes in phe-

nologies have already been observed in the life cycles of

terrestrial plants (Amano et al. 2010), animals (Bradshaw

and Holzapfel 2006) and some freshwater fish (e.g. earlier

spring spawning of grayling and roach in Switzerland—

Gillet and QueTin 2006; Wedekind and Kung 2010 and

walleye in North America—Schneider et al. 2010). These

relatively rapid adjustments of spawning phenology to

local warming are likely phenotypic responses (Bradshaw

and Holzapfel 2006) to temporal shifts in water tempera-

ture cycles (e.g. Elliott and Elliott 2010). Such adjustments

are limited by the genetically determined photoperiod cues

that establish the spawning window for a species (Brad-

shaw and Holzapfel 2007, Hendry and Day 2005). De-

synchronization of the typical seasonal temperature cycle

from the fixed annual photoperiod cycle can lead to de-

synchronization (or abnormal synchronization) of a wide

range of co-dependent biological phenologies with delete-

rious consequences for many of the organisms involved,

particularly in systems with high amplitude seasonal pro-

duction cycles (Donnelly et al. 2011). For fish, a common

consequence would be significant increases in egg and

larval mortality. In fall spawners, this can stem from fac-

tors such as exposure to higher, harmful temperatures in

fall (Casselman 2002) and premature hatching in spring

that leads to a mismatch between initiation of larval

feeding and the start of the spring production pulse (Pörtner

and Peck 2010). De-synchronization of matched feeding

phenologies (and vice versa) among younger and older fish

can also change inter-specific interactions from predation

to competition (and vice versa) with significant conse-

quences for both growth and survival (Borcherding et al.

2010). In spring river spawners, de-sychronization of the

typical flood cycle from the fixed photoperiod cycle may

have similar effects on species that use the timing of the

first spring flood as the proximate cue to initiate spawning

migrations. Such increases in larval mortality will impose

intense selection pressures on photoperiod cuing systems,

with the species that respond rapidly to those pressures

being the species that are best able to persist and prosper in

such altered habitats (Casselman 2002; Bradshaw and

Holzapfel 2010).


123

Ta

ble

2E

colo

gic

alan

dev

olu

tio

nar

yim

pac

tso

fth

ech

ang

esin

win

ter

con

dit

ion

sex

pec

ted

fro

mg

lob

alcl

imat

ech

ang

e

Ch

ang

ein

win

ter

con

dit

ion

s

Gro

up

affe

cted

Imm

edia

teim

pac

tsM

ediu

m-t

erm

imp

acts

Lo

ng

-ter

mim

pac

ts

Red

uce

d

du

rati

on

So

uth

ern

po

pu

lati

on

s

of

cold

-wat

er

spec

ies

Ov

eral

lg

row

ing

seas

on

sho

rten

san

db

eco

mes

dis

con

tin

uo

us,

wit

hsu

mm

er

per

iod

incr

easi

ng

lych

arac

teri

zed

by

nee

dfo

rre

fug

esfr

om

hig

h

tem

per

atu

res

and

low

ox

yg

enle

vel

s

Red

uce

dp

red

atio

no

np

rey

spec

ies

Red

uce

dab

un

dan

ce

Po

siti

ve

effe

cts

on

abu

nd

ance

of

pre

y

spec

ies

Lo

cal

exti

nct

ion

sle

adin

gto

ran

ge

con

trac

tio

n

Res

ult

ant

emp

tyn

ich

esin

crea

se

vu

lner

abil

ity

of

imp

acte

d

foo

dw

ebs

toin

vas

ion

s

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rth

ern

po

pu

lati

on

s

of

coo

lan

dw

arm

wat

ersp

ecie

s

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ng

erg

row

ing

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on

Incr

ease

dp

red

atio

no

np

rey

po

pu

lati

on

s

Incr

ease

dab

un

dan

ce

Neg

ativ

eef

fect

so

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dan

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fp

rey

spec

ies

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ge

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on

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eral

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iver

sity

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ease

sin

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cted

by

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ge

exp

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on

Ch

ang

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nu

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nt

cycl

ing

,

wat

erq

ual

ity

and

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tam

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t

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mu

lati

on

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ort

er

tran

siti

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s

to/f

rom

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mer

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lan

dsp

rin

g

spaw

ner

s

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ease

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mp

ora

lo

ver

lap

insp

awn

ing

tim

eso

fsy

mp

atri

csp

ecie

sIn

crea

sed

inte

rbre

edin

gam

on

gcl

ose

ly

rela

ted

spec

ies

Intr

og

ress

ion

lead

ing

tolo

cal

exti

nct

ion

s

Sp

ecia

tio

n

Incr

ease

dte

mp

ora

lo

ver

lap

of

spec

ies-

spec

ific

larv

alfi

rst

feed

ing

tim

es

Incr

ease

dco

mp

etit

ion

for

avai

lab

lefo

od

reso

urc

es

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ease

dv

aria

bil

ity

inan

nu

al

recr

uit

men

tle

adin

gto

incr

ease

d

var

iab

ilit

yin

po

pu

lati

on

abu

nd

ance

Sh

ifts

insp

ecie

sd

iver

sity

Lat

ero

nse

t/

earl

ier

term

inat

ion

Fal

lan

dsp

rin

g

spaw

ner

s

Des

yn

chro

niz

atio

no

fth

ety

pic

alan

nu

alw

ater

tem

per

atu

re(a

nd

riv

erfl

oo

d)

cycl

efr

om

the

fix

edan

nu

alp

ho

top

erio

dcy

cle

dis

rup

tslo

cal

accl

imat

ion

of

larv

alfi

rst

feed

ing

tim

esto

the

tim

ing

of

the

ann

ual

pro

du

ctio

np

uls

e

Incr

ease

dv

aria

bil

ity

info

od

reso

urc

esav

aila

ble

atfi

rst

feed

ing

for

fish

larv

ae,

cou

ple

dw

ith

incr

ease

dco

mp

etit

ion

for

tho

sere

sou

rces

that

are

avai

lab

le

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ease

dv

aria

bil

ity

inan

nu

al

recr

uit

men

tle

adin

gto

incr

ease

d

var

iab

ilit

yin

po

pu

lati

on

abu

nd

ance

Sh

ifts

insp

ecie

sd

iver

sity

Str

on

gse

lect

ion

for

gen

etic

chan

ges

insp

awn

ing

cuin

g

syst

ems

Ch

ang

ein

inte

nsi

tyo

f

spri

ng

flo

od

s

Fal

lsp

awn

ers

Ch

ang

esin

var

iab

ilit

yo

feg

g/l

arv

alm

ort

alit

yC

han

ges

inv

aria

bil

ity

of

ann

ual

recr

uit

men

t,le

adin

gto

chan

ges

in

var

iab

ilit

yo

fp

op

ula

tio

nab

un

dan

ce

Sh

ifts

insp

ecie

sd

iver

sity

See

rev

iew

sb

yB

rad

shaw

and

Ho

lzap

fel

(20

10

),M

cGin

n(2

00

2),

Pört

ner

and

Pec

k(2

01

0),

So

mer

o(2

01

0)

for

det

ails


123

Table 2 provides a summary of the more likely impacts

on fish communities of the changes in winter phenology

expected with climate change.

Conclusion

The annual occurrence of low water temperatures, accom-

panied by low prey densities, has shaped the behavioural

repertoire and physiological characteristics of many of the

freshwater fish species that are endemic to the colder

regions of the Northern Hemisphere. Of these species,

winter specialists (e.g. many salmonids) are coldwater-

adapted, spawn in fall, actively feed during winter and

avoid the high summer temperatures found in the epilimnia

of temperate lakes. Future climatic trends promise to rap-

idly shorten northern winters, rendering redundant many of

the ecological specializations that characterize the species

native to these environments. This will occur over a time

frame that may be too short for these species to effectively

adapt to the new conditions. Even if some adaptation can

occur, local extinction of winter specialists is likely in many

locations because of the accessibility of these systems to

invading cool- and warmwater species that will out-com-

pete resident winter specialists in these newly benign

environments. Thus, future climate change will likely result

in range contractions along the southern zoographic

boundaries of winter specialist species. In regions where

watershed connections (or other forces assisting species

dispersal) exist, maintenance or even enhancement of fish

biodiversity may occur as species that are adapted to less

stringent environmental conditions invade and exclude

winter specialists from the niches they currently occupy.

Acknowledgments We would like to thank Christof Engelhardt,Georgiy Kirllin and Heike Zimmermann-Timm for organizing the

Winter Limnology Meeting in Liebenburg and the participants for the

stimulating atmosphere. We thank P. Abrams, S. Cooke, J. Magnuson,

C. K. Minns and H. A. Regier for their insightful reviews of earlier

drafts of the manuscript. Support for this work was provided by the

Climate Change Program of the Ontario Ministry of Natural

Resources, the Natural Sciences and Engineering Research Council of

Canada and the University of Toronto.

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