The Role of Winter Phenology in Shaping the Ecology of Freshwater ﬁsh and Their Sensitivities to Climate Change

Aquat Sci (2012) 74:637–657 DOI 10.1007/s00027-012-0274-3 Aquatic Sciences

OVERVIEW

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

B. J. Shuter • A. G. Finstad • I. P. Helland • I. Zweimu¨ller • F. Ho¨lker

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

Abstract Thermal preference and performance provide zoogeographic distribution of a species covers a broad the physiological frame within which fish species seek range of winter conditions, local populations may exhibit strategies to cope with the challenges raised by the low differences in their winter survival strategies that reflect temperatures and low levels of oxygen and food that adaptation to local conditions. Extreme winter specialists characterize winter. There are two common coping strate- are found in shallow eutrophic lakes where long periods of gies: active utilization of winter conditions or simple ice cover cause winter oxygen levels to drop to levels that toleration of winter conditions. The former is typical of are lethal to many fish. The fish communities of these lakes winter specialist species with low preferred temperatures, are simple and composed of species that exhibit specialized and the latter is typical of species with higher preferred adaptations for extended tolerance of very low tempera- temperatures. Reproductive strategies are embodied in the tures and oxygen levels. Zoogeographic boundaries for phenology of spawning: the approach of winter conditions some species may be positioned at points on the landscape cues reproductive activity in many coldwater fish species, where the severity of winter overwhelms the species’ while the departure of winter conditions cues reproduction repertoire of winter survival strategies. Freshwater fish in many cool and warmwater fish species. This cuing communities are vulnerable to many of the shifts in envi- system promotes temporal partitioning of the food resour- ronmental conditions expected with climate change. ces available to young-of-year fish and thus supports Temperate and northern communities are particularly high diversity in freshwater fish communities. If the vulnerable since the repertoires of physiological and behavioural strategies that characterize many of their members have been shaped by the adverse environmental B. J. Shuter conditions (e.g. cool short summers, long cold winters) that Harkness Laboratory of Fisheries Research, climate change is expected to mitigate. The responses of Ontario Ministry of Natural Resources, Peterborough, Canada these strategies to the rapid relaxation of the adversities B. J. Shuter that shaped them will play a significant role in the overall Department of Ecology and Evolutionary Biology, University responses of these fish populations and their communities of Toronto, 25 Harbord Street, Toronto M5S3G5, Canada to climate change. A. G. Finstad I. P. Helland Norwegian Institute for Nature Research, P.O. Box 5685, Keywords Thermal performance Bioenergetics Sluppen, 7485 Trondheim, Norway Survival strategies Zoogeographic boundaries Climate change Winter kill I. Zweimu¨ller Department of Evolutionary Biology, Faculty of Life Sciences, University of Vienna, Vienna, Austria Introduction F. Ho¨lker (&) Leibniz Institute of Freshwater Ecology and Inland Fisheries, 12587 Berlin, Germany In the northern hemisphere, the time frame that winter e-mail: [email protected] occupies in the annual round of seasons varies widely from 123 638 B. J. Shuter et al. place to place and from year to year. This variable ‘phenology’ 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 Fig. 1 Illustration of continental (Europe—stippled vs. North Amer- ica—cross hatched) differences in how latitude influences the start available. Since winter is the season when prey are scarce (solid boundary lines) and end (dashed boundary lines) of the ice (or inaccessible), changes in winter phenology can cause cover period for a typical lake. Day zero is Jan 1. Values were derived large changes in fish growth and reproduction. In North using the physical limnological model FLAKE (Kirillin et al. 2011) America, the south to north climatic gradient of shorter 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 summers and longer winters is accompanied by systematic reflect variation expected over a range in longitude from 20oEto changes in population characteristics (e.g., spawning time, 30oE; North American regions reflect variation expected over a range somatic growth, size and age at reproduction, lifespan) of in longitude from -75oWto-100oW many freshwater fish species (e.g. Dunlop and Shuter 2006; Zhao et al. 2008; McDermid et al. 2010; Venturelli for temperate freshwater fish. We have based our review on et al. 2010). Similar links between fish life history char- the authors’ familiarity with the relevant literature, sup- acteristics and climate gradients have been noted in plemented by a systematic Web of Science search of papers Europe and South America (Heibo et al. 2005; Lappalai- published from Jan 2006 thru Feb 2012 using topic key nen and Tarkan 2007; Finstad et al. 2010), and in marine words ‘winter’ and ‘fish’. fish species (Po¨rtner 2006). We begin by discussing the functional trade-offs faced The characteristics of winter phenology that are of by fish that must live with different winter phenologies. We particular importance for fish are its start and end dates and then give an overview of the bioenergetic context that its overall duration (e.g. Shuter and Post 1990). To illus- defines many of the strategies developed by fish to deal trate how these characteristics vary geographically, we with winter. We continue by classifying fish species with adopt the following, somewhat simplistic (but clear and respect to their thermal tolerances, link these tolerances to unambiguous) definition of winter: winter is the period of both winter survival- and reproductive strategies, and ice cover for a water body (lake or river). This definition illustrate the potential for intraspecific variation in these provides us with clear measures for winter start, end and strategies. We show that winter conditions and thermal duration. It also isolates those ecosystems that experience tolerances are tightly linked to the zoogeographic bound- the full set of adverse conditions outlined above, from aries of many freshwater fish species and we discuss some those that experience a moderated subset, conditioned by of the processes generating high mortalities at these annual minimum light levels that are not impeded by ice boundaries and consequent shifts in fish community com- cover. We use the physical limnological model FLAKE position. Finally, we argue that our categorization of winter (Kirillin 2010; Kirillin et al. 2011) and climatic conditions survival strategies highlights the relative sensitivities of for the years 2005–6 to illustrate the geography of ‘winter’ different freshwater fish species to climate change and conditions for a typical lake, and how that geography dif- adds to the growing list of characteristics that make fers between North America and Europe (Fig. 1). temperate freshwater ecosystems particularly vulnerable to In the present paper, we provide a conceptual overview the impacts of climate change (Jeppesen et al. 2010; of current knowledge on the challenges that winter poses Woodward et al. 2010).

123 Winter phenology, freshwater ﬁsh and climate change 639

Winter phenology and ﬁsh survival Physiology constrains winter strategies

The challenges of winter Fish are ectotherms and hence their ability to interact with their environment, and acquire energy for growth and In temperate latitudes, the phenology of the seasons gen- reproduction, strongly depends on temperature. There is an erates wide annual variation in light, temperature, oxygen extensive literature describing how the performance of a and food resources and this variation poses significant fish changes when it is exposed to different temperatures trade-off challenges (Fig. 2). A common objective for all (Fry 1971; Elliott 1976; Magnuson et al. 1979; Ohlberger species and life stages is to allocate available energy to et al. 2008a; Hasnain et al. 2010). Several metrics (e.g. maximize individual survival and reproductive success. For preferred temperature, upper and lower lethal tempera- most species, individuals accumulate energy over spring- tures) have been developed to characterize these effects summer-fall and deplete it during winter (Shuter and Post and all of these metrics are strongly correlated, exhibiting 1990). Winter depletion is particularly acute for early life associations that are similar for both marine and freshwater stages, since the weight-specific capacity to store energy species (Fig. 3). These correlations suggest that each fish decreases with decreasing body size, while weight-specific species is adapted to perform optimally over a specific energy expenditure increases (Shuter and Post 1990; Ultsch range of temperatures. This is a common property of 1989). Increased winter mortality, resulting from exhaus- ectotherms and its physiological foundation is presented in tion of energy reserves, has been reported among the early several recent reviews (Clarke and Po¨rtner 2010;Po¨rtner life stages of a wide variety of species (e.g. smallmouth 2010;Po¨rtner et al. 2010). This foundation can be bass Micropterus dolomieui—Oliver et al. 1979; perch summarized as follows: the species-specific range of tem- Perca fluviatilis and flavescens—Post and Evans 1989; peratures that best supports acquisition of energy from the Huss et al. 2008; white perch Morone americana—Johnson environment is bounded by the upper and lower pejus and Evans 1991; rainbow trout Oncorhynchus mykiss— temperatures; these landmark temperatures define a tem- Biro et al. 2004b; Atlantic salmon Salmo salar—Finstad perature ‘window’ over which the aerobic scope (the et al. 2004a; roach Rutilis rutilus—Knopf et al. 2007). difference between the highest and lowest rates of aerobic Adult individuals have two additional challenges associ- respiration) is high and relatively constant. The optimal ated with winter: first, how to acquire and store the growth temperature and the preferred temperature are additional energy necessary to produce viable larvae, and typically shifted toward the upper end of this window second, how to ensure that the temporal placement of lar- (Po¨rtner 2010). The utility of this definition of an ecolog- vae permits them to acquire the maximum benefit from the ically relevant thermal window (an ERTW) has recently summer pulse of food resources. In the following sections, been confirmed in a study demonstrating that temporal we discuss constraints on the strategies that are commonly fluctuations in the abundance of eelpout (Zoarces vivipa- used to meet all of these challenges. We then go on to rous) in the North Sea were strongly linked to changes in discuss the strategies themselves. the degree to which environmental temperatures fell within

Fig. 2 Schematic illustration of Temperature Oxygen the ‘challenge of winter’: the energy needed to survive winter Light intensity high: Light intensity low: food scarcity and successfully Prey abundant & visible Prey sparse & invisible reproduce must be acquired during the limited period of summer food abundance Growth Possible Starvation Likely

Ice Absent Ice Present

Day

123 640 B. J. Shuter et al.

(i) Upper • Species with high preferred temperatures will be Lethal inefﬁcient energy gatherers under winter conditions 35 (e.g. warmwater species such as smallmouth bass— (ii) Optimal Shuter and Post 1990; Suski and Ridgway 2009a) Growth • species with low preferred temperatures will be more 25 efﬁcient energy gatherers under winter conditions (e.g. coldwater species such as Atlantic salmon—Finstad 15 et al. 2004b) (iii) Lower • the time and energy needed to re-tool enzyme systems Lethal to improve performance under winter conditions (i.e. the costs of acclimation) will decrease with decreases in 5 the difference between preferred and winter tempera-

Critical thermal metrics (°C) tures (Po¨rtner 2006) -5 Thus, we suggest that the costs of developing physio- 5 15 25 logical strategies to maintain energy acquisition under Preferred temperature (°C) winter conditions will be lower for species with lower preferred temperatures. We also suggest that the impetus Fig. 3 Thermal performance metrics for freshwater and marine fish. Freshwater species (data from Hasnain et al. 2010): (1) Upper lethal (i.e. the selection pressure) to develop such strategies will temperature versus preferred temperature: dashed line = geometric increase with increases in the relative duration of winter mean regression of upper lethal temp on preferred temperature; over summer: at low latitudes, where winter duration is stars = individual species. (2) Optimal growth temperature versus short, the impetus should be weak and it should increase preferred temperature: solid line = geometric mean regression of optimal growth temperature on preferred temperature; closed cir- progressively with the increases in relative winter dura- cles = individual species. Marine species (data from Tsuchida 1995; tion that accompany increases in latitude (Fig. 1). Also, Po¨rtner and Peck 2010): the light-shaded region is bounded by the increases in winter duration are typically accompanied by relationships linking upper (i) and lower lethal temperatures (iii) to declines in summer surface water temperatures (Shuter preferred temperature. The dark-shaded region illustrates Magnu- son’s definition (preferred temperature ±2 C) of an ecologically et al. 1983). As a consequence, the annual period of opti- relevant thermal window (ERTW) mal performance for a typical species (i.e. the period when environmental temperatures fall within its ERTW) should the ERTW for eel pout (e.g. Po¨rtner and Knust 2007). Fur- also change with increases in latitude—its duration short- ther support for this concept can be found in inter-population ening for warmwater species and extending for coldwater studies of freshwater fish based on Magnuson et al. (1979) species (Fig. 4). Therefore, the impetus to develop spe- simple, empirical definition of the ERTW for a species (i.e. cialized adaptations that support energy acquisition during its ‘fundamental thermal niche’ = the species-specific pre- winter should be strongest in environments that are most ferred temperature ± 2 C—see Fig. 3). Christie and supportive of coldwater species (Fig. 4). This is consistent Regier (1988) used an asymmetric variant of this definition with our finding (Table 1) that species with low preferred (i.e. a 4 C window centred 1 C below the species-specific temperatures typically feed under winter conditions, and preferred temperature: a definition that should be quantita- hence may be considered winter specialists. In contrast, tively similar to the more precise definition proposed by species with high preferred temperatures are often quies- Po¨rtner) and found that, for each of four freshwater fish cent during winter, thus exhibiting a strategy of tolerating, species (Salvelinus namaycush, Coregonus clupeaformis, rather than exploiting, winter conditions. Energy storage Sander vitreus and Esox lucius) with very different preferred and husbanding strategies are common to most species that temperatures (10–24 oC), population productivity increased have been studied (Table 1). with increases in the annual amount of time that water temperatures fell within the species’ ERTW. Bioenergetics shape the ecological context for winter Most freshwater (and marine) fish have a preferred strategies temperature [4 oC (Fig. 3), yet the maximum temperature available during winter is typically B4 oC. Enzymatic For organisms living in seasonal environments, an indi- specialization to a particular temperature range is costly vidual’s behaviour will respond to seasonal changes in the and broadening that range could compromise performance abiotic and biotic factors that surround it. Bioenergetics in the neighbourhood of the optimal temperature (DeWitt provide a functional framework, with a standardized and Wilson 1998;Po¨rtner et al. 2006). Hence it is rea- energetic currency, which permits these short and long- sonable to suggest that: term responses to be rationalized in terms of coherent

123 Winter phenology, freshwater ﬁsh and climate change 641

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 allocated 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, individual characteristics (e.g. sex, size, age, stored energy Fig. 4 Effect of increasing latitude on: (1) the annual duration of levels), competition with other individuals and various optimal performance for two species with different preferred environmental characteristics, both biotic and abiotic temperatures (25 and 10 C). The duration of optimal performance is the time (% of ice-free season) that lake surface water temperature (Lester et al. 2004; Shuter et al. 2005). The total metabolic remains within the ERTW for the species (Magnuson’s definition: expenditure is bounded by the aerobic metabolic scope and preferred temperature ± 2 C); (2) the ratio of ice-free days to ice hence is continually being reshaped by those aspects of the cover days: the impetus to develop specialized strategies for energy abiotic environment (temperature, oxygen levels, pH) that acquisition under winter conditions. The dependence of the lake surface water temperature regimes on latitude was derived from the strongly affect aerobic scope (Po¨rtner 2010). North American FLAKE simulations summarized in Fig. 1 The energy available to the individual depends on the overall intake of energy from foraging, [I - (MSDA ? hypotheses linking physiological, ecological and evolu- F ? U)], offset by the cost of foraging itself (included in tionary factors (e.g. Kitchell et al. 1977; Jobling 1994; Ma). Both of these elements will vary widely across sys- Hanson et al. 1997). The study of bioenergetics involves tems and species. For a visual feeder, the energy intake the examination of energy gains and losses, and the transfer (I) from foraging will vary directly with light intensity (L), of energy within the whole organism. Ingested energy is the density of prey resources (R) and the level of foraging partitioned into the major physiological components lead- activity. The level of foraging activity itself will depend ing to the universal energy budget equation (Jobling 1994): on: DE=I ðÞM+P+U+F ð1Þ (i) temperature (T): the maximum possible foraging rate will increase with aerobic scope and therefore will The energy balance of the fish (DE) is the difference increase with increases in T, peak as T enters and between energy ingested as food (I) and the sum of the remains within the ERTW for the species, and then energy: (1) expended by metabolic processes (M), (2) decline as T increases beyond the species’ ERTW invested in tissue growth (P), (3) lost in the form of (Po¨rtner 2010); partially oxidized products excreted as urea (U), (4) lost in (ii) standard metabolism (M ): the higher the standard faeces (F). s metabolism, the greater the daily energetic demand The primary components of this energy budget can be that must be met by foraging; higher demand will partitioned into different subunits. The energy costs of drive higher levels of foraging in order to keep the metabolic processes can be partitioned as: probability of death by starvation low (Lima and Dill M ¼ M þ M þ M þ M ð2Þ s SDA a PL 1990; Huckstorf et al. 2009); where Ms is the standard, or basal metabolic rate and (iii) metabolic cost of supporting parasite load (MPL): consists of the metabolic costs associated with maintaining parasites are not usually lethal to their fish hosts but the viability of existing body mass, MSDA (i.e. the specific they often cause tissue pathology and substantial

123 642 B. J. Shuter et al.

Table 1 Species-speciﬁc examples of different winter survival strat- preferred temperatures \*15 C; warmwater species with preferred egies, grouped by preferred temperature along lines suggested by the temperatures [*25 C; cool water species with intermediate values 3 thermal guilds of Magnuson et al. (1979): coldwater species with Winter survival Preferred temperature strategy \12 12–18 18–24 [24

Energy storage Arctic charr (Finstad et al. Atlantic salmon (Berg et al. Striped bass Atlantic silverside (Schultz and Conover 2003), 2010; (Hurst and 1997), Burbot (Winter storage, Finstad et al. 2010), Rainbow Conover 2003; Mosquito ﬁsh (Reznick and Braun 1987), Ho¨lker et al. 2004) trout (Biro et al. 2004b; Hurst et al. 2000), Smallmouth bass (Mackereth et al. 1999), Post and Parkinson 2001) European perch Roach (van Dijk et al. 2005) (Huss et al. 2008), European perch (Heermann et al. 2009), Gizzard shad (Ultsch 1989)

Active: Arctic charr (Finstad et al. Whiteﬁsh (Siikavuopio et al. Pike (Kobler et al. White bass (Cooke et al. 2003), Roach Feeding ? risk 2003), 2010), 2008a), (Bro¨nmark et al. 2008) avoidance Coregonus fontanae, Atlantic salmon (Cunjak White crappie Corgonus albula (Helland 1996; Finstad et al. 2010, (Tschantz et al. et al. 2007), 2004a, b; Linnansaari et al. 2002) Lake trout (Blanchﬁeld et al. 2008), 2009), Brown trout Brook trout (Cunjak and (Amundsen and Knudsen Power 1986) 2009)

Active- Ruffe (Ho¨lker and Thiel 1998) Yellow perch Green sunﬁsh (Kolok 1991; Tschantz et al. Quiescent (Johnson and 2002), Evans 1991; Bluegill (Shoup and Wahl 2011; Tschantz Ultsch 1989), et al. 2002; Ultsch 1989), Black crappie Pikeperch (Kirjasniemi and Valtonen (Cooke et al. 1997; Lappalainen and Vinni 2001; 2003; Tschantz Vehanen and Lahti 2003; Teletchea et al. 2002) et al. 2009), Roach (van Dijk et al. 2005;Ho¨lker and Breckling 2005; Binner et al. 2008), Bream (Ho¨lker 2006)

Quiescent Burbot (summer Blacknose dace Smallmouth bass (Shuter et al. 1989; Kolok quiescence-(Hardewig (Ultsch 1989) 1991; Barthel et al. 2008; Suski and et al. 2004; Finstad et al. Ridgway 2009b), 2010) Largemouth bass (Lemons and Crawshaw 1985; Hanson et al. 2008; Tschantz et al. 2002; Hasler et al. 2009a, b), Pumpkinseed (Evans 1984), Carp (Ultsch 1989), Brown bullhead (Lemons and Crawshaw 1985; 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), Coregonus fontanae, 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 Winter phenology, freshwater ﬁsh and climate change 643

metabolic stress, thus imposing an additional meta- Inet = I –(Msda + F + U) bolic cost on the host (Lemly and Esch 1984; Knopf E initial et al. 2007; Seppanen et al. 2008); MPL increases with parasite load and consequently increases the

obligate daily energetic demand (Ms ? MPL); higher M = demand will drive higher levels of foraging in order a Inet to keep the probability of death by starvation low; (iv) prey resources (R): as prey density increases, the

Stored energy Stored M > I E a net M < I level of foraging activity will begin to decline, since crit a net Toleration strategy optimal: Specialization strategy optimal: increases in density will lead to increases in the foraging provides no benefit foraging beneficial proportion of each feeding period that the individual * spends digesting food, as well as decreases in the net T surv energy the individual will gain for each unit of Time energy expended on foraging (Holling 1959); (v) predation risk (PR): increases in predation risk (e.g. from Fig. 5 Schematic illustrating how the usefulness of active feeding under winter conditions is determined by: (1) the pre-winter level of increased predator density) are typically accompanied stored energy (Einitial) and the minimum level required to maintain by a decline in the optimal level of foraging activity, viability (Ecrit); (2) the ingestion rate (I) and the energetic losses since lower foraging activity typically decreases expo- associated with that ingestion rate (Ma,MSDA, F, U); (3) the obligate sure to predation and hence offsets increases in predation energy demand (Ms ? MPL). These factors determine the expected lifetime (T ) under winter conditions. In the absence of feeding, the risk (Biro et al. 2004a; Chiba et al. 2007); surv expected lifetime (T*surv) is determined jointly by the energy storage Therefore, the energy intake rate (I) will depend on L, T, levels and the obligate energy demand: T*surv = (Einitial-Ecrit)/ (Ms ? MPL). In situations where the energetic cost of active foraging (Ms ? MPL), R and PR. Now, if [Ma] is larger or smaller (Ma)is[the net energy gained from foraging (Inet), then foraging (i.e. =) than [I - (MSDA ? F ? U)], the activity costs provides no benefit: use of stored energy is[(Ms ? MPL) and Tsurv is associated with foraging will be greater, or less, than the \T*surv. In such situations, the optimal strategy is to cease feeding energy that foraging provides. These bioenergetic and adopt a toleration strategy. In situations where foraging is beneficial (Ma \ Inet), then the optimal strategy is to engage in winter inequalities shape the ways in which ecological factors (L, foraging as part of a specialization strategy. The optimal foraging rate T, PL, R, PR) drive the cost-benefit tradeoff that deter- would be subject to the degree of predation risk—if an increase in mines the realized level of winter foraging activity. predation risk causes a drop in expected lifetime, then the animal During winter, negative energy budgets are common and should reduce foraging activity so as to reduce its exposure to this increased risk risk of starvation mortality is high because: (i) negligible rates of primary production under low Dealing with winter: strategies for survival light and temperature conditions lead to low prey and reproduction densities; (ii) the net energy gain from active, visual foraging is Strategies for dealing with winter reductions in light, often negative because of the longer search times, temperature and prey resources fall into three broad cate- and consequently higher activity costs, required to gories: toleration, specialization, and reproduction. The successfully capture prey when both light levels and first two deal with individual survival over winter, while prey densities are low; the latter deals with offspring survival. Figure 5 illustrates (iii) the overall benefit from active foraging may be two different strategies for managing activity to increase reduced due to increased predation risk from preda- winter survival, given a fixed level of stored energy in fall. tors that are adapted to low temperature conditions If conditions are such that the energy depletion rate under (e.g. endotherms, cold-adapted ectotherms); optimal foraging provides no net gain in energy (Ma C (iv) temperatures may reach levels low enough to evoke [I - (MSDA ? F ? U)]), then, at best, the energy depletion physiological inhibition of foraging activity. rate will equal the rate associated with no foraging (Ms ? MPL) and the animal will receive no benefit from its The expected lifetime for a fish with a negative energy exposure to the level of predation risk associated with budget depends on the overall rate of energy depletion, the foraging. In this situation, the best winter survival strategy initial level of pre-winter energy storage (Einitial), and the will always be to cease foraging, thus reducing both met- critical minimum storage level needed for survival (Ecrit). abolic costs and predation risk. This is one aspect of a The rate of energy depletion is set by the difference toleration survival strategy. Conversely, if the optimal between metabolic costs and energy intake. Death ensues foraging rate can sustain a net energy gain to the organism when energy levels fall to E (Fig. 5). crit (Ma \ [I - (MSDA ? F ? U)]), then the storage depletion

123 644 B. J. Shuter et al.

rate will be reduced and the expected lifetime (Tsurv, Facultative and obligate controls on winter energy usage Fig. 5) will be extended. Under these conditions, the have been observed in many fish species. Obligate reduc- optimal winter survival strategy will be to forage at a rate tions in basal metabolism, cued by the reductions in that provides the optimal trade off between the mortality photoperiod that precede winter, have been identified in risks from starvation and predation (Bull et al. 1996). This several temperate freshwater fish species (Beamish 1964; is a specialization survival strategy. Evans 1984). Facultative behaviour that serves to minimize Toleration strategies include both the pre-winter storage activity metabolism during winter is also common. This of energy for winter use (Berg et al. 2009; Hurst and Co- typically involves selection of microhabitats (e.g. boulders, nover 2003) and the minimization of demands on that stored groundwater inflows, deeper areas in the water column) energy during winter (Evans 1984; Shuter et al. 1989). with reduced exposure to high and/or variable water cur- Specialization strategies focus on continuing energy rents. Many studies of river and lake systems have reported acquisition during winter (Ho¨lker et al. 2004; Finstad et al. such behaviours. The winter use of sheltered areas (e.g. 2010). Reproductive strategies focus on timing reproduc- deep water areas, pools, side channnels) has been observed tion to ensure effective access by larvae to the summer for cyprinids (Heermann and Borderding 2006; Irmler et al. production pulse (Yeates-Burghart et al. 2009; Migaud et al. 2008; Rakowitz et al. 2009), salmonids (Cunjak and Power 2010;Po¨rtner and Peck 2010). Toleration and specialization 1986; Swales et al. 1986) and a variety of other species strategies are of particular importance for juvenile fish since (e.g. Esox lucius Kobler et al. 2008b). Studies of brook they typically experience higher winter mortality risk trout Salvelinus fontinalis (Cunjak and Power 1986) con- because of their higher mass specific metabolic rates and cluded that typical over-wintering behaviour was lower lipid storage capacities (Ultsch 1989; Shuter and Post consistent with a strategy of choosing habitats to minimize 1990). Reproductive strategies are the province of mature energy costs. All of these diverse examples of winter adults and are designed to maximize offspring survival, habitat selection can be interpreted as vehicles for reducing potentially at the expense of parental survival. both swimming cost and predation risk. States of extreme inactivity during winter have been Toleration survival strategies observed in a variety of fish species. Animals in such a quiescent state typically remain in sheltered habitats, There are two common toleration strategies: energy storage exhibit minimal movements and do not feed (Lemons and prior to winter and minimization of energy usage during Crawshaw 1985; Shuter et al. 1989). However, they may winter. remain active in the absence of sheltering habitats (Shuter Energy storage is a widespread adaptation to seasonality et al. 1989) and still respond to direct stimuli—they do not (e.g. Schultz and Conover 1997; Finstad et al. 2010). exhibit the obligate entry into a deep torpid state that is Energy reserves are typically acquired in times of abundant typical of hibernating ectotherms such as turtles and lizards food supply or where physical conditions support adequate (Ultsch 1989). Comparative studies of the physiology of physiological performance of the individual (Hurst 2007). quiescent-winter species and active-winter species have Fish commonly store energy reserves in the form of non- found that quiescent species: polar lipids (Jobling 1994) and for temperate freshwater (i) do not exhibit the hypertrophy of heart and liver fishes, this usually takes place during summer and fall (e.g. typical of winter acclimation in active species Hurst and Conover 2003). There are many studies docu- (Tschantz et al. 2002); menting accumulation of energy storage products in (ii) have a smaller scope for cardiac output than active juvenile fish (van Dijk et al. 2005), and similar behaviour species (Cooke et al. 2003); has been documented in a few studies of adults (Dawson (iii) exhibit a significantly larger drop in basal metabolic and Grimm 1980; Adams et al. 1982; Encina and Granado- rate and spontaneous activity under winter conditions Lorencio 1997). Lipids and glycogen are usually the first than is expected, given the temperature difference reserves to be mobilized when food becomes scarce (Shi- between summer and winter (Lemons and Crawshaw meno et al. 1990; Sargent et al. 2002;Ho¨lker and Breckling 1985; Tschantz et al. 2002); this drop may reflect 2005). However, with extended periods of starvation, these anticipatory reductions in basal metabolic rate trig- reserves will become depleted and then liver and muscle gered by declining photoperiod (Evans 1984). 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 Specialization survival strategies species, is the winter utilization for maintenance metabolism of ovarian energy, originally allocated to egg Fish can adapt their behaviour and physiology to increase development (Henderson et al. 1996, 2000). their success during stressful periods, and some species are 123 Winter phenology, freshwater fish and climate change 645 better adapted to winter stresses than others. Species that a growth efficiency (per unit of food) that is almost twice perform well during winter may be regarded as ‘‘winter that of brown trout (Salmo trutta), a closely related species specialists’’. Following the bioenergetic framework with similar thermal performance parameters and food described above, winter ‘specialists’ are those species that preferences (Finstad et al. 2011; Helland et al. 2011). are proficient at both capturing prey under winter condi- These potentially competing coldwater species coexist in tions and converting captured prey biomass to useable many lakes across northern Europe. Their ability to coexist energy. This is achieved through adaptations to low light, may be founded on species-specific sets of contrasting low prey abundance, low temperatures and, in some sys- seasonal adaptations that translate into a pattern of reci- tems, low oxygen levels. procal competitive advantage—the aggressive, energy Fish living at high latitudes with severe winters and demanding behaviour of brown trout giving it a competi- short days seem capable of detecting very low light levels. tive advantage over arctic charr during the summer period For example, studies of several species in both Norway of prey abundance, while the superior winter feeding (Strand et al. 2008) and Finland (Jurvelius and Marjomaki abilities and conversion efficiencies of arctic charr make it 2008) have shown that diel behaviour patterns driven by the superior competitor during winter when prey are rare day-night cycling continue unimpeded in waters covered (Finstad et al. 2011). by thick layers of ice and snow. Successful feeding in Some species are strictly cold-adapted and stay in cold reduced light can be achieved by improving vision or by lake habitats at all times of the year. One example of an employing other senses that do not depend on light (e.g. extremely cold-adapted fish is Coregonus fontanae,a mechano-reception or chemoreception—Janssen and species endemic to Lake Stechlin in northern Germany and Corcoran 1993; Liang et al. 1998). In lakes with long ice- closely related to the more common European vendace (C. cover and deep snow cover, species that are less dependent albula). Coregonus fontanae has a preferred temperature of on light for feeding will have a competitive advantage over 4.2 C and its swimming performance is optimal at about visual feeders. However, for many fish, the effect of 4 C (Ohlberger et al. 2008a, b). It remains in deep waters ambient light on capture success is probably less critical throughout the year and hence always experiences winter- than the low resource biomass found in such lakes because like temperatures of 4–6 C (Mehner et al. 2010). Another of their low levels of primary production. example of an extreme winter specialist is burbot (Lota Some salmonids benefit from ice-cover and have poorer lota), a species that is most active in winter and exhibits performance during ice-free winter periods (Finstad et al. little movement in summer (Ho¨lker et al. 2004). At higher 2004c; Helland et al. 2011). This is probably related to summer temperatures, its feeding and basal metabolic rates increased predation risk in ice-free conditions, causing are reduced, it seeks physical shelter and its energy stores individuals to reduce their foraging times. Another factor is are depleted (Binner et al. 2008; Nagel et al. 2011). During metabolism, which is reduced in darkness under ice-cover winter, it is an efficient benthivorous and piscivorous but remains high in the absence of ice due to heightened predator (Lehtonen 1998) and its energy stores are refilled activity. The result is a net loss of energy because food (Binner et al. 2008; Nagel et al. 2011). It may be advan- levels are too low to permit the increases in consumption tageous for burbot to exhibit this unusual strategy of high needed to maintain the heightened activity. Arctic charr are hunting and feeding activity during winter because most of found at higher latitudes than any other freshwater fish its potential competitors are relatively inactive and hence species and are therefore the species most likely to exhibit burbot would experience reduced interspecific food com- specific adaptations for surviving under conditions where petition and lower predation risk (Ho¨lker et al. 2004). winters are long and productivity is low. Laboratory studies of charr have found them capable of growing at very low Reproductive strategies temperatures (*2-5 C : Larsson et al. 2005) while field and laboratory studies have shown that they feed throughout Many temperate freshwater fish species have a single long periods of ice-cover (Klemetsen et al. 2003; Svenning spawning period annually (Scott and Crossman 1973), and and Klemetsen 2007; Amundsen and Knudsen 2009) and that period is typically placed at either the start (fall can exhibit over-winter growth (Siikavuopio et al. 2010). spawners) or the end (spring spawners) of winter. For many Size classes that have grown large enough to switch their North American freshwater fish, the timing of spawning is diet from zooplankton to benthic invertebrates may feed directly linked to thermal performance: fish with low pre- better over winter since winter abundance of benthic ferred temperatures (coldwater fish) spawn in the fall and invertebrates can be much greater than zooplankton abun- fish with higher preferred temperatures (cool/warmwater dance (Bystro¨m et al. 2006;Ho¨lker 2006). fish) spawn in the spring (Fig. 6). Timing is regulated by a To benefit from feeding at low prey densities, a high cuing system based on photoperiod and temperature, such food conversion efficiency is required and arctic charr have that spawning can only occur within a time window (spring 123 646 B. J. Shuter et al.

Fig. 6 Phenology of reproduction for fall and spring spawning fish. Each box plot gives the optimal spawning, egg development and growth temperatures for these two reproductive classes of fish. The solid-shaded regions mark the two periods in a year when surface water temperatures lie within the ERTW of the fall spawner. The hatched-shaded region marks the single period in a year when surface water temperatures lie within the ERTW of the spring spawner. The data summarized in the box plots are from a compilation of thermal performance metrics for Canadian freshwater fish species (Hasnain et al. 2010). Units for all box plots are C

or fall) defined by photoperiod, but the exact date within temperature somewhat below the preferred temperature, this window is determined by the date when water tem- adults are able to utilize all of the fall feeding period to peratures exceed a species-specific spawning temperature gather energy for expenditure on reproduction; (Bradshaw and Holzapfel 2007). Given a broad time win- (iii) performance of warmwater fish typically exceeds that dow and a fixed spawning temperature, the spawning date of coldwater fish during the period of warmer for a widely distributed spring spawner should vary directly temperatures that hold during much of the production with latitude and this has been observed for several Euro- pulse; therefore, spring spawning, at a temperature pean species (Lappalainen and Tarkan 2007). Among somewhat below the preferred temperature, permits North American freshwater fish, the spawning temperature rapid embryo development during spring/early sum- itself is typically *5 C less than the preferred tempera- mer so that larvae can begin feeding during periods ture for both spring and fall spawners (Fig. 6). This pattern when both their feeding efficiency and food avail- can be rationalized as follows: ability is high; in addition, this affords adults the opportunity of ‘assessing’ the severity of winter as it (i) the timing of spawning should be adjusted to permit proceeds and ‘deciding’ whether to skip spawning larvae to maximize the benefit they can gain from the and use the energy stored in reproductive products for annual summer production pulse; self maintenance (Henderson et al. 1996). (ii) performance of coldwater fish typically exceeds that of warmwater fish during the low temperatures that This linkage between thermal performance and the precede and follow the annual production peak; timing of spawning leads to temporal partitioning of the hence fall spawning, with consequent slow embryo food resources available to young-of-year fish during the development under winter temperatures, permits the annual production pulse. Such partitioning limits compe- larvae of coldwater fish to hatch and begin feeding at tition among species that differ widely in thermal the start of the production pulse when low temper- performance and thus supports the wide diversity in ther- atures maximize their efficiency at using the food mal performance typical of the fish communities found in available; in addition, by positioning the spawning deeper temperate zone lakes.

123 Winter phenology, freshwater ﬁsh and climate change 647

Inter- and intra-specific variation in winter strategies of local adaptation in both storage and reproductive strategies are evident in the recent literature (Yeates-Burghart Most species exhibit some form of energy storage strategy et al. 2009; Finstad et al. 2010; Berg et al. 2011). However, (Table 1). Even extreme winter specialists such as burbot there are limits to the effectiveness of some strategies. For utilize this strategy, with winter replacing summer as the example, a pure toleration strategy, consisting of energy season of storage accumulation (Ho¨lker et al. 2004; Nagel storage and winter quiescence, must become increasingly et al. 2011). However, inter-specific variation in other ineffective with the joint increases in winter length and winter strategies is extensive and, as expected, exhibits decreases in summer production that accompany increases strong links with thermal performance: there is an in latitude. Thus winter may play a significant role in increasing emphasis on quiescent strategies among species shaping the zoogeographic boundaries of some species. with higher preferred temperatures (Table 1) and the seasonal timing of spawning is strongly linked to thermal performance (Fig. 6). These associations are not rigid— Winter strategies overwhelmed: the location some euryoecious species can deploy variants of several of zoogeographic boundaries strategies. For example, roach will engage in winter migrations between lake and river environments, balancing The northern zoogeographic boundaries of some species growth opportunities against predation risk (Bro¨nmark may be shaped by the presence of winter conditions severe et al. 2008) but, when migration is impossible, they will enough to overwhelm the strategies available for coping adopt an opportunistic-quiescent strategy with respect to with them. Shuter and Post (1990) showed that the current foraging: they will abandon active foraging but will positions of the northern zoogeographic boundaries for opportunistically feed on prey that enter their refuge hab- smallmouth bass and yellow perch in North America could itats (Ho¨lker and Breckling 2005). Similarly, smallmouth be explained directly in terms of how their phenologies of bass will elect a quiescent strategy in the presence of refuge reproduction, growth and winter energy usage depend on habitats but will adopt active predator avoidance behaviour the phenology of winter. They also listed several other (i.e. schooling) in their absence (Shuter et al. 1989). species that might be similarly affected. Studies of some With respect to reproductive strategies, there are marine species suggest that similar considerations may be exceptions to the link between thermal performance and shaping their northern distributional boundaries (Conover spawning timing, but they are not inconsistent with the and Present 1990;Po¨rtner and Peck 2010). Since both the rationale outlined above. For example, spring spawning costs of coping with winter (Figs. 2 and 3) and the strate- morphs of arctic charr exist in both England and Norway gies for dealing with it (Table 1; Fig. 6) are linked to (Frost 1965; Klemetsen et al. 1997). However, these are thermal performance, we might expect to find a relatively deep profundal morphs experiencing more or less constant simple link between measures of thermal performance and temperatures of 4 C, year-round and in the English pop- the position of distributional boundaries. Shuter et al. ulation, they represent only a very small proportion (2002) showed that, for a large subset of North American (*4 %) of the adults (Baroudy and Elliot 1994). There are fish, species with higher preferred temperatures exhibited also some exceptional populations within the Coregonus northern distributional boundaries that were associated albula complex. Fall spawning is typical for most popu- with warmer longer summers and shorter winters. We lations, but some populations spawn in winter or spring extended the analyses of these data to ask the more specific (Vuorinen et al. 1981; Mehner et al. 2010, 2012). These question of whether the positions of these northern distri- populations appear to have diverged from ancestral fall butional boundaries were associated with the fraction of the spawners, in response to intense selection pressure imposed ice-free period when surface water temperatures were on zygotes and juveniles by adverse winter oxygen con- within the ERTW of each species (Fig. 7). We found that ditions (Vuorinen et al. 1981). these northern distributional boundaries were located For species with broad geographic distributions, con- where annual water temperature regimes provided minimal siderable intra-specific variation in winter strategies is exposure to temperatures that lie within species-specific expected. As the level of winter stress increases along the ERTW’s. climatic gradient found within a species’ range, selective An interesting corollary to this analysis is that, for pressures should act to strengthen its elected winter sur- southern lakes, a significant portion of the ice-free period vival strategies. Trends of this sort have been noted in exhibits surface temperatures that are optimal for cold- marine species (Conover et al. 2005) and might be adapted fish (Fig. 7). These temperatures are found in the expected to be stronger in freshwater limnetic species, ‘shoulder’ seasons of spring and fall and they are sufficient where the constraints on gene flow imposed by watershed to support viable populations of these species provided isolation should favour local adaptation. Indeed, examples that: 123 648 B. J. Shuter et al.

40 20°C among driving variables likely generate the ‘fuzzy’ edges A 15°C 10°C that characterize the zoogeographic boundaries for many 30 25°C freshwater ﬁsh species (e.g. Shuter et al. 1980). Another important abiotic factor is winter oxygen 20 availability, which varies with both lake morphometry and winter duration. In shallow eutrophic lakes, long winters

performance 10 Duration optimal

(% ice free season) can lead to mass mortalities of ﬁsh and other biota (i.e. 0 winter-kill events) due to severe oxygen depletion in late B winter. Such events are caused (Greenbank 1945) by: (1) 30 25°C ice cover stopping inputs of atmospheric oxygen to the lake; (2) ice, and especially snow cover, cutting off light 20 20°C and thus stopping oxygen inputs from photosynthesis; (3) 15°C Preferred temperature 10 consumption of available oxygen, particularly near the lake bottom, by biological degradation of organic matter. The

40 50 60 70 Latitude degree of oxygen depletion will vary directly with increa- 12.5 4.5 -3.4 -11 Mean annual ses in summer productivity, length of ice cover and benthic air temperature (°C) water temperature, and inversely with increases in lake Latitude/Climate at boundary depth and the ratio of lake volume to benthic-surface-area Fig. 7 a For North America: the association between increasing (Fang and Stefan 2000; Meding and Jackson 2001; Clilverd latitude and the annual duration of optimal performance for species et al. 2009; Liboriussen et al. 2011). Mortality among with preferred temperatures of 25, 20, 15 and 10 C. The duration of resident biota will be augmented by additional by-products optimal performance is the time (% of ice-free season) lake surface water temperatures remain within the ecologically relevant thermal of biological degradation, such as toxic gases (hydrogen window for the species (Magnuson’s definition: preferred sulphide, methane) and carbon dioxide, and can be exac- temp ± 2 C). Lake surface water temperatures were generated from erbated by biological factors such as fungal (Bly et al. the FLAKE simulations for North America illustrated in Fig. 1; mean 1993) and bacterial infection (Hayman et al. 1992), stress annual air temperature at each latitude is consistent with the FLAKE simulations. b Preferred temperatures for 23 North American fish (O’Connor et al. 2010), parasite load and age (Kennedy species plotted against the latitude marking the northern zoogeo- et al. 2001). Winter-kill is a common phenomenon among graphic boundary for each species (see Shuter et al. 2002 for details). shallow lakes in regions characterized by long winters (e.g. Block arrows illustrate the fact that, for each temperature preference Alaska—Clilverd et al. 2009; Alberta—Danylchuk and class, the typical latitude marking the northern zoogeographical boundary for species belonging to the class corresponds to the latitude Tonn 2003; Eaton et al. 2005; Danylchuk and Tonn 2006; at which duration of optimal performance for the class falls to zero. Finland—Ruuhijarvi et al. 2010). Greenbank (1945) esti- The striped bar marks the range of latitudes that separate the mated the annual risk of occurrence for a lake typical of the continental land mass from the Arctic Ocean Michigan lakes he studied to be *0.33 year-1 while Magnuson et al. (1998) estimated the risk for individual Wisconsin lakes to range from 0.05 to 0.2 year-1.In (i) the lake stratifies in summer, does not exhibit hypolim- central Europe, the risk is much lower (e.g. Geiger 1962 netic oxygen depletion during stratification and thus reported no winter kills in Switzerland over a 10 year provides a coldwater summer refuge to sustain the period). However, the impact of even a single winter kill population (Evans 2007; Blanchfield et al. 2009); event can have long lasting effects on the lake that expe- (ii) the lake does not stratify, but surface temperatures do riences it (e.g. Ridgway et al. 1990; Eaton et al. 2005). not reach lethal levels and the fish is free of Lakes that are subject to frequent winter kill events competitors with higher preferred temperatures typically support a unique community of fish species that (Gunn 2002; Mackenzie-Grieve and Post 2006). possess a range of specialized behavioural and physiolog- The relationships between thermal metrics and bound- ical strategies for tolerating winter oxygen deficits (Tonn aries (Fig. 7) are relatively loose, with much unexplained et al. 1990). Where winters are very long and low oxygen variation. This variation likely reflects the influence of a levels are common and persistent, toleration strategies fail broad range of abiotic and biotic factors that modify the and fishless lakes become common (Jackson et al. 2007). In influence of climatic conditions on the aquatic environ- such lakes, the zooplankton and phytoplankton communi- ment. For example, systematic differences in lake size and ties, and the annual pattern of nutrient cycling, differ morphometry can generate systematic differences in both widely from what is common in lakes that support fish ice phenology and summer water temperatures despite communities (Jackson et al. 2007; Balayla et al. 2010; common climatic conditions. These sorts of interactions Jeppesen et al. 2010).

123 Winter phenology, freshwater ﬁsh and climate change 649

Winter strategies for tolerating oxygen deficits: make them vulnerable to the impacts of climate change species endemic to winter-kill lakes (Woodward et al. 2010). The vulnerability of these ecosystems is accentuated by the fact that they are populated The survival strategies that permit food acquisition under by fish species whose behavioural and physiological winter conditions are paralleled by the specialized oxygen strategies have been shaped by the need to deal with deficit strategies of the fish species that persist in winter- adverse winter conditions. The responses of these strategies kill lakes. In Wisconsin, winter-kill lakes are characterized to the rapid relaxation of the adversities that shaped them by a unique community of fish species (Klinger et al. 1982; will play a significant role in the overall impact of climate Magnuson et al. 1985) that exhibit a range of simple change on these ecosystems. adaptations for tolerating low oxygen conditions: migration Decreases in the duration of ice cover will progressively to high-oxygen micro-refuges, orientation to higher oxygen reduce the competitive advantage that winter specialists concentrations at the ice-water interface and morphological have over eurythermal species (Po¨rtner 2006), promoting adaptations that permit the direct breathing of air trapped in both decreases in their local abundance and contractions of bubbles at the ice-water interface. In Finland, the crucian their distributional ranges (e.g. Finstad et al. 2011; Helland carp (Carassius carassius L.) is often the only fish species et al. 2011; Ulvan et al. 2012). This will be exacerbated by found in lakes that are susceptible to winter-kill. This the difficulties that winter specialists will face in dealing species has adapted to life in low oxygen conditions by with the epilimnetic summer warming that will accompany developing an efficient anaerobic respiratory system shorter winters (Po¨rtner 2006; Somero 2010). Rapid (Holopainen et al. 1986; Nilsson and Renshaw 2004). warming may overwhelm the ability of such organisms to Such oxygen deficit specialists are often the only species effectively adapt to these changes, although recent work that can persist in lakes that are subject to frequent winter- (Salinas and Munch 2012) suggests that some fish species kill events. These same species are rare or absent in lakes have adaptive mechanisms (e.g. transgenerational plasticity that do not suffer from winter-kill events. It seems likely of optimal growth temperature) that can operate on quite that this presence/absence pattern stems from the fact that short time scales. The potential impact that the disappear- the costs and inefficiencies associated with winter oxygen ance of winter may have on winter specialists generally is deficit strategies become a sufficient burden in more benign most clearly seen in the disjunct distributions of species environments to prevent successful competition with the adapted to persist in winter-kill systems—these winter wide range of species that can live in those benign specialists are rare or absent in those systems that are free environments. 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 Sensitivity to climate change is shaped by winter Northern Hemisphere began in the 1980’s (e.g. Meisner strategies et al. 1987; Shuter and Post 1990; Shuter and Meisner 1992) and are continuing (e.g. Sharma et al. 2007). These Historical trends in the climate of the Northern Hemisphere studies consistently predict that the northern boundaries for have been accompanied by significant changes in the warmwater (e.g. smallmouth bass Micropterus dolomieu) phenology of ice cover in both lakes and rivers (North and coolwater fish (e.g. yellow perch Perca flavescencs and America: Magnuson et al. 2000; Lemke et al. 2007; Benson European perch Perca fluviatilis) will extend northward et al. 2012. Europe: Livingstone 1997; Stonevicius et al. over the period 2000–2100. In contrast, coldwater species 2008; Weyhenmeyer et al. 2008. Asia: Smith 2000; Batima are expected to undergo habitat reductions (e.g. Salvinus et al. 2004; Vuglinski 2006). Current trends (e.g. Trenberth Alpinus—Gerdeaux 2011; Salvelinus namaycush—Gunn et al. 2007) and future projections (e.g. Christensen et al. et al. 2004; Salvelinus fontinalis—Meisner 1990; Coreg- 2007) suggest that, over the next century, winter duration onus artedi—Sharma et al. 2011) along the southern will decrease progressively and winter phenology will shift boundaries of their zoogeographic distributions. In the in concert with that decrease. These changes will be deeper lakes along these southern boundaries, cold hypo- accompanied by increases in summer surface water tem- limnetic waters provide summer refuges for coldwater peratures and shifts in the thermocline depth of lakes. species. Extensions of the stratification period in some of Significant changes in both lake water levels and river flow these lakes (particularly eutrophic lakes) will lead to severe rates are also likely, with the direction of change (increase and pervasive hypolimnetic oxygen deficits in late summer. or decrease) depending as much on climatic region (e.g. This will reduce/eliminate such refuges, leading to reduc- maritime vs mid-continent) as on absolute change in air tions in abundance of the local populations that rely on temperature. The freshwater ecosystems resident in these them (Stefan et al. 2001; Plumb and Blanchfield 2009) and water bodies share a wide range of characteristics that ultimately to contractions in the zoogeographic ranges of 123 650 B. J. Shuter et al. these species. Most of this work has focused on North study of climate change impacts on French rivers suggested American distributions; however, a recent empirical study that species diversity would increase more than trait of the occurrence and relative density of Eurasian diadro- diversity in many locations, leading to increases in the mous species found that approximately 20 % of the species overall intensity of competition for resources (e.g. food— examined were sensitive to changes in winter conditions Vander Zanden et al. 1999). Such shifts could, for example, (Lassalle and Rochard 2009). cause increased hybridisation rates due to increased com- If changes in winter phenology promote range exten- petition for spawning sites resulting from greater overlap in sions for both cool and warmwater fish, then fish species species-specific spawning times. richness should increase in many parts of the north tem- In addition to changing limnetic and riverine fish habi- perate zone (e.g. Meisner et al. 1987). Recent studies of tat, changes in winter phenology will also lead to changes distributional changes in French rivers are consistent with in the phenology of fish life cycles. Such changes in phe- such predictions: in most locations, fish species richness nologies have already been observed in the life cycles of increased, warm-water fish species new to the area were terrestrial plants (Amano et al. 2010), animals (Bradshaw observed and most native species exhibited habitat and Holzapfel 2006) and some freshwater fish (e.g. earlier expansions (Daufresne and Boet 2007). Trends toward spring spawning of grayling and roach in Switzerland— increased richness may be blocked or reversed in those Gillet and QueTin 2006; Wedekind and Kung 2010 and locations where changes in climate are accompanied by walleye in North America—Schneider et al. 2010). These changes in the frequency and severity of winter floods relatively rapid adjustments of spawning phenology to (Trenberth et al. 2007). Given the extensive use of river local warming are likely phenotypic responses (Bradshaw habitats by limnetic fish populations for spawning sites, and Holzapfel 2006) to temporal shifts in water tempera- nursery areas and winter refuges, any systematic change in ture cycles (e.g. Elliott and Elliott 2010). Such adjustments the frequency and/or intensity of winter floods could have are limited by the genetically determined photoperiod cues significant impacts on populations of these species, as well that establish the spawning window for a species (Brad- as on populations of riverine fish. For example, Doll and shaw and Holzapfel 2007, Hendry and Day 2005). De- Zhang (2010) predicted a decrease in fish species richness synchronization of the typical seasonal temperature cycle in those rivers where discharge rates will decrease due to from the fixed annual photoperiod cycle can lead to de- climate change. Such decreases are predicted for only a synchronization (or abnormal synchronization) of a wide few rivers, but some of these are located in biogeograph- range of co-dependent biological phenologies with delete- ically valuable regions (e.g. the Amazon basin). rious consequences for many of the organisms involved, Changes in species richness can cause many other eco- particularly in systems with high amplitude seasonal pro- logical effects. Perhaps the most extreme effects forecast in duction cycles (Donnelly et al. 2011). For fish, a common the literature involve those associated with the relaxation of consequence would be significant increases in egg and winter kill conditions in shallow fertile lakes. Together larval mortality. In fall spawners, this can stem from fac- with the expected shifts in zoogeographic boundaries, this tors such as exposure to higher, harmful temperatures in will open up new habitats for colonization by fish and other fall (Casselman 2002) and premature hatching in spring long lived aquatic vertebrates over broad geographic areas, that leads to a mismatch between initiation of larval leading to shifts in nutrient cycles, changes in the seasonal feeding and the start of the spring production pulse (Po¨rtner cycling of phytoplankton and zooplankton biomass and and Peck 2010). De-synchronization of matched feeding changes in water quality that are typically associated with phenologies (and vice versa) among younger and older fish eutrophy (e.g. increased turbidity, higher chlorophyll lev- can also change inter-specific interactions from predation els, increased prevalence of cyanophyta, Jackson et al. to competition (and vice versa) with significant conse- 2007; Balayla et al. 2010; Jeppesen et al. 2010; Sorensen quences for both growth and survival (Borcherding et al. et al. 2011). At higher trophic levels, initial increases in 2010). In spring river spawners, de-sychronization of the richness will promote changes in predation and competi- typical flood cycle from the fixed photoperiod cycle may tion pressures that can strongly affect final community have similar effects on species that use the timing of the composition. Sharma et al. (2007) argued that increased first spring flood as the proximate cue to initiate spawning predation by invading smallmouth bass would pose a migrations. Such increases in larval mortality will impose serious threat to native cyprinid species (as per Jackson intense selection pressures on photoperiod cuing systems, 2002), while Ng and Gray (2011) argued that climate dri- with the species that respond rapidly to those pressures ven shifts in predator–prey relationships could cause being the species that are best able to persist and prosper in increased bioaccumulation of persistent chemicals in such altered habitats (Casselman 2002; Bradshaw and freshwater food chains. Buisson and Grenouillet’s (2009) Holzapfel 2010).

123 itrpeooy rswtrﬁhadciaechange climate and ﬁsh freshwater phenology, Winter

Table 2 Ecological and evolutionary impacts of the changes in winter conditions expected from global climate change Change in Group affected Immediate impacts Medium-term impacts Long-term impacts winter conditions

Reduced Southern populations Overall growing season shortens and becomes discontinuous, with summer Reduced abundance Local extinctions leading to duration of cold-water period increasingly characterized by need for refuges from high Positive effects on abundance of prey range contraction species temperatures and low oxygen levels species Resultant empty niches increase Reduced predation on prey species vulnerability of impacted food webs to invasions Northern populations Longer growing season Increased abundance Range expansion of cool and warm Increased predation on prey populations Negative effects on abundance of prey Overall diversity increases in water species species food webs affected by range expansion Changes in nutrient cycling, water quality and contaminant bioaccumulation

Shorter Fall and spring Increased temporal overlap in spawning times of sympatric species Increased interbreeding among closely Introgression leading to local transitions spawners related species extinctions to/from Speciation summer Increased temporal overlap of species-speciﬁc larval ﬁrst feeding times Increased variability in annual Shifts in species diversity Increased competition for available food resources recruitment leading to increased variability in population abundance

Later onset/ Fall and spring Desynchronization of the typical annual water temperature (and river flood) Increased variability in annual Shifts in species diversity earlier spawners cycle from the fixed annual photoperiod cycle disrupts local acclimation recruitment leading to increased Strong selection for genetic termination of larval first feeding times to the timing of the annual production pulse variability in population abundance changes in spawning cuing Increased variability in food resources available at first feeding for fish systems larvae, coupled with increased competition for those resources that are available

Change in Fall spawners Changes in variability of egg/larval mortality Changes in variability of annual Shifts in species diversity intensity of recruitment, leading to changes in spring variability of population abundance ﬂoods See reviews by Bradshaw and Holzapfel (2010), McGinn (2002), Po¨rtner and Peck (2010), Somero (2010) for details 123 651 652 B. J. Shuter et al.

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