Hemispheric-scale patterns of climate-related shifts in ...post.queensu.ca/~pearl/Planktonic/Ruhland et al 2008 GCB.pdfHemispheric-scale patterns of climate-related shifts in planktonic

Hemispheric-scale patterns of climate-related shiftsin planktonic diatoms from North American andEuropean lakes

K AT H L E E N R U H L A N D *, A N D R E W M . PA T E R S O N w and J O H N P. S M O L *

*Paleoecological Environmental Assessment and Research Laboratory (PEARL), Department of Biology, Queen’s University,

Kingston, ON, Canada K7L 3N6, wDorset Environmental Science Centre, Ontario Ministry of the Environment,

1026 Bellwood Acres Road, Dorset, ON, Canada P0A 1E0

Abstract

A synthesis of over 200 diatom-based paleolimnological records from nonacidified/

nonenriched lakes reveals remarkably similar taxon-specific shifts across the Northern

Hemisphere since the 19th century. Our data indicate that these diatom shifts occurred in

conjunction with changes in freshwater habitat structure and quality, which, in turn, we

link to hemispheric warming trends. Significant increases in the relative abundances of

planktonic Cyclotella taxa (Po0.01) were concurrent with sharp declines in both heavily

silicified Aulacoseira taxa (Po0.01) and benthic Fragilaria taxa (Po0.01). We demonstrate

that this trend is not limited to Arctic and alpine environments, but that lakes at

temperate latitudes are now showing similar ecological changes. As expected, the onset

of biological responses to warming occurred significantly earlier (Po0.05) in climatically

sensitive Arctic regions (median age 5 AD 1870) compared with temperate regions

(median age 5 AD 1970). In a detailed paleolimnological case study, we report strong

relationships (Po0.005) between sedimentary diatom data from Whitefish Bay, Lake of

the Woods (Ontario, Canada), and long-term changes in air temperature and ice-out

records. Other potential environmental factors, such as atmospheric nitrogen deposition,

could not explain our observations. These data provide clear evidence that unparalleled

warming over the last few decades resulted in substantial increases in the length of the

ice-free period that, similar to 19th century changes in high-latitude lakes, likely

triggered a reorganization of diatom community composition. We show that many

nonacidified, nutrient-poor, freshwater ecosystems throughout the Northern Hemisphere

have crossed important climatically induced ecological thresholds. These findings are

worrisome, as the ecological changes that we report at both mid- and high-latitude sites

have occurred with increases in mean annual air temperature that are less than half of

what is projected for these regions over the next half century.

Keywords: climate, Cyclotella, ice-out, meta-analysis, Northern Hemisphere lakes, paleolimnology,

planktonic diatoms

Received 8 January 2008; revised version received 16 April 2008 and accepted 23 April 2008

Introduction

Unequivocal evidence of pronounced warming in high

latitude and high altitude regions beginning in the 19th

century is well documented (Moritz et al., 2002; ACIA,

2004). Similarly, air temperatures in temperate latitudes

of the Northern Hemisphere have increased over the

last century, with an amplification of this warming

trend over the past 30–40 years that is unprecedented

in the last �1300 years (Jansen et al., 2007).

The effects of recent temperature increases on fresh-

water ecosystems may be blurred at temperate lati-

tudes, as these regions are typically subjected to

multiple stressors that can mask or override climatic

signals (Smol, 2008). However, in remote regions where

extensive anthropogenic disturbances are diminished,

the effects of climatic fluctuations on physical, biologi-

cal and chemical processes of freshwater ecosystems are

more clearly evident (Schindler et al., 1996; Gerten &Correspondence: John P. Smol, tel. 1 1 613 533 6147, fax 1 1 613

533 6617, e-mail: [email protected]

Global Change Biology (2008) 14, 2740–2754, doi: 10.1111/j.1365-2486.2008.01670.x

r 2008 The Authors2740 Journal compilation r 2008 Blackwell Publishing Ltd

Adrian, 2002). Although the nature and magnitude of

climate-driven responses may vary among freshwater

systems, it is clear that a warmer climate will affect

important lake properties and thus aquatic biota in a

myriad of complex ways (Keller, 2007).

Analyses of spatial synchrony (i.e. temporal coher-

ence) in lake ecosystem responses to climatic changes

have rarely been examined at a regional or global scale.

Given the wide range of differences in geographic set-

tings, atmospheric circulation patterns and various feed-

back mechanisms, the temporal and spatial consistency

of biological responses to these climatic changes is not

expected. Furthermore, regional and site-specific differ-

ences in lakes (e.g. lake morphology, depth, bedrock

geology) can result in a variety of responses, even under

large-scale climatic changes. However, recent studies

have reported strong correlations between plankton dy-

namics and climate variables (North Atlantic Oscillation,

El Nino-Southern Oscillation Index) in lakes in North

America and Europe (Straile & Adrian, 2000; Weyhen-

meyer et al., 2002; Blenckner et al., 2007; Rusak et al.,

2008). Thus, despite differences among lake settings and

characteristics, regional climatic drivers may result in

significant coherence among lakes within bioregions.

In many dimictic lakes, siliceous algae, particularly

diatoms (Bacillariophyceae), are an important compo-

nent of seasonal phytoplankton maxima, the timing of

which may play a key role in the success of zooplankton

populations (e.g. Winder & Schindler, 2004a; Adrian

et al., 2006). Numerous climate-related physical proper-

ties in lakes, such as the length of the open-water season,

the timing, duration and strength of thermal stratifica-

tion, the timing and strength of the spring freshet, and

the duration of spring overturn play critical roles in algal

dynamics and community structure. These lake proper-

ties, in turn, affect water-column mixing processes, light

availability and stability, and nutrient distribution (Smol,

1988). For example, warmer temperatures (quite notably

winter temperatures) have resulted in earlier ice-out

dates, earlier onset of thermal stratification, and earlier

development of diatom blooms in both European (e.g.

Adrian et al., 2006) and North American (e.g. Winder &

Schindler, 2004b) lakes. Changes in the abundance and

composition of primary producers in lakes can directly

impact abundances of slower growing zooplankton taxa

(Adrian et al., 2006), with important implications for

cascading effects throughout aquatic foodwebs (Winder

& Schindler, 2004b).

Recent increases in the relative abundances of small

Cyclotella species, concurrent with decreases in heavily

silicified Aulacoseira species and/or small, benthic

Fragilaria taxa, were originally linked to warming-

related changes in lakes from subarctic regions of

Finland (Sorvari & Korhola, 1998; Sorvari et al., 2002)

and Canada (Ruhland et al., 2003; Ruhland & Smol, 2005).

Recently, paleolimnological studies from temperate re-

gions across Canada (e.g. Werner et al., 2005; Harris et al.,

2006) have likewise reported increases in planktonic

Cyclotella species that we found to be strikingly similar

to the above subarctic studies. However, a global synth-

esis of these trends has hitherto not been undertaken. The

emergence of this recurring pattern in taxon-specific

changes in lakes from diverse ecological settings

prompted us to examine these trends more closely.

Plankton-based studies (e.g. sediment traps, water-

column sampling, monitoring data, surface sediments)

have added valuable insights into the seasonal dynamics

of various plankton groups including species-level

diatom trends. Although generally short in duration

(typically 2 years or less), these empirical studies have

found climate-related patterns in Cyclotella–Aulacoseira–

Fragilaria diatom assemblages that may be related to the

length of the ice-free season, the timing, duration and

strength of thermal stratification, the depth of the mixed

epilimnion, the duration of the mixing period, and/or

subsurface habitat development in relation to these

factors (e.g. Fahnenstiel & Glime, 1983; Kilham et al.,

1996; Raubitschek et al., 1999; Lotter & Bigler, 2000;

Rautio et al., 2000; Ptacnik et al., 2003; Chu et al., 2005;

Forsstrom et al., 2005; Pannard et al., 2008). In general,

these studies have concluded that warming-induced

lakewater properties favor small Cyclotella species (Cyclo-

tella comensis/gordonensis, Cyclotella stelligera/pseudostelli-

gera/glomerata) over larger and heavier Aulacoseira

species and/or small benthic Fragilaria diatom species.

Longer-term monitoring data (�20–30 years) are rare,

and when they exist rarely measure algal assemblages

beyond coarse taxonomic groupings. While these studies

clearly show that climate has played an important role in

the composition of phytoplankton in freshwater lakes

over the last few decades (e.g. Findlay et al., 2001), there

is unfortunately little or no information on diatom sea-

sonal dynamics at the species level.

In this paper, we provide a meta-analysis of more

than 200 diatom-based paleolimnological studies that

explores the geographic extent, spatial synchrony, and

possible mechanisms for recent taxon-specific shifts (i.e.

Cyclotella–Aulacoseira–Fragilaria species) recorded in a

wide variety of Northern Hemisphere lakes. Specifi-

cally, we ask: (1) How many diatom-based paleolimno-

logical profiles contain significant populations of

Cyclotella species? (2) How many of these profiles record

an increase or decrease in the relative abundance of

Cyclotella species in recent sediments, and what do

these lakes have in common? (3) Do studies that record

increases in Cyclotella show concurrent decreases in

Aulacoseira and/or Fragilaria species? (4) What is the

geographic extent and timing of this increasing Cyclo-

P L A N K T O N I C D I AT O M R E S P O N S E S T O R E C E N T WA R M I N G 2741

r 2008 The AuthorsJournal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, 14, 2740–2754

tella trend? (5) What are the most plausible mechanisms

for this taxon-specific diatom shift? Furthermore,

we examined a high-resolution diatom record from

Whitefish Bay (Lake of the Woods, Ontario, Canada) in

relation to long-term climate records, lake ice records,

and atmospheric nitrogen deposition to elucidate the

primary driver of this taxon-specific diatom shift (e.g.

climate, habitat change, atmospheric contaminants). We

conclude that nonacidified/nonenriched lakes from

both circum-Arctic and temperate regions are showing

remarkably similar warming-induced taxon-specific

shifts since the 19th century. Diatom responses to

warming were most sensitive in Arctic lakes but as

temperature-related thresholds were exceeded at lower

latitudes during the mid-20th century, this ecological

reorganization is now evident throughout the Northern

Hemisphere.

Methods

Paleolimnological studies containing Cyclotella species:meta-analysis

Biological proxy data preserved in lake sediments pro-

vide a reliable means for assessing ecological response to

long-term environmental change (Smol, 2008). In parti-

cular, subfossil diatoms have been a mainstay for paleo-

limnological assessments because of their ability to

respond rapidly to environmental change, their siliceous

frustules preserve well, and their wide distribution

among a diverse array of aquatic habitats (Stoermer &

Smol, 1999). Dated, continuous lake-sediment sequences

(i.e. lake-sediment records examined at close, consecutive

intervals for the full core length) provide valuable re-

cords of the timing, magnitude, and direction of environ-

mental change based on changes in diatom assemblages

preserved in the sediment (Stoermer & Smol, 1999).

We recognize that not all lake types will support the

particular diatom taxa examined in this study (i.e. Cyclo-

tella–Fragilaria–Aulacoseira: Appendix S1) and, in addi-

tion to the genera considered here, other diatom species

may also be sensitive to climatically induced limnologi-

cal changes (e.g. see Smol et al., 2005). For example,

recent studies from both the Russian Arctic, as well as

in the Experimental Lakes Area (ELA; Ontario, Canada),

have also reported increases in the relative abundances

of planktonic diatoms, but these include genera such as

Asterionella and Tabellaria with concurrent decreases in

Aulacoseira taxa over the past few decades [Smol et al.,

2005; Solovieva et al., 2005, 2008; M. Enache (National

Academy of Sciences, Philadelphia, PA), personal com-

munication]. These shifts may also be the result of recent

warming with Asterionella and Tabellaria dominating the

water column when stratification is strongest at the end

of summer, and Aulacoseira taxa dominating in early

spring with blooms occurring under ice (Solovieva

et al., 2005). However, it was not practical for us to

examine all available diatom records that elicit a re-

sponse to climate. Rather, we have restricted our study

to paleolimnological data that specifically contain the

word ‘Cyclotella’ in published manuscripts, theses, or

consultant reports, and that contain Cyclotella in recent

sedimentary profiles (last ca. 200 years).

An important criterion for our meta-analysis was that

lakes included in this study must not be profoundly

disturbed by human activities so as to eliminate some of

the more important confounding factors, such as high

nutrient concentrations and low pH. For example, lakes

in which concentrations of total phosphorus (TP) are

420mg L�1 are more apt to experience cyanobacterial

algal blooms than more oligotrophic lakes (MOE, 1994).

Similarly, a pH level below 6 is found to be the point at

which an ecological threshold is passed whereby acid-

related aquatic community changes become measurable

(e.g. Holt et al., 2003). Therefore, we categorized lakes as

not being profoundly affected by cultural disturbances

as having concentrations of TP 20 mg L�1 or less and that

pH levels must be 6.0 or higher. These criteria also

included lakes that are currently showing a recovery

from these impacts. For example, many lakes in both

Europe and North America have undergone intensive

remediation programs initiated in the early 1970s in

response to eutrophication of freshwater systems from

the addition of phosphorus and nitrogen compounds.

As a result of these remediation efforts, many of these

lakes are starting to show some recovery over the last

decade or more. We rationalize that once these pollution

stressors have been sufficiently removed, ambient cli-

matic signals would become prevalent on the diatom

assemblages from these systems.

All manuscripts included in our analysis were tabu-

lated, irrespective of whether or not these studies

registered increases, decreases or no trend in the rela-

tive abundances of small, planktonic Cyclotella taxa

through time. Diatom-based paleolimnological studies

that were included in this meta-analysis conformed to

the following criteria. (1) All detailed diatom profiles

had an established chronology (e.g. 210Pb dating) for the

last ca. 200 years; (2) all continuous diatom records

contained at least 2% relative abundance of Cyclotella

species in at least one sedimentary interval; (3) all detailed

cores, as well as ‘top-bottom’ regional paleolimnological

analyses, included lakes with present TP measurements

below 20 mg L�1 and pH above 6 (i.e. lakes unimpacted

by anthropogenic nutrient enrichment or acid deposi-

tion). This criterion eliminated lakes with confounding

factors as described above. (4) Diatom profiles were

categorized as showing a rise in Cyclotella species if this

2742 K . R U H L A N D et al.


increase was greater than 5% above background relative

abundances.

We examined differences in the timing of the diatom

changes in lakes among regions [i.e. high latitude, high

altitude, low latitude (temperate)] using an ANOVA on

ranks followed by Dunn’s post hoc test to examine pair-

wise differences. Study lakes were categorized by region

based on the original authors’ classifications; Arctic and

subarctic lakes were considered to be high latitude. The

approximate timing (year) of the change was determined

from the authors’ interpretations, or by directly examin-

ing the published diatom stratigraphies and estimating

the point at which the relative abundance of Cyclotella

exceeded 5% above background levels (i.e. beyond the

estimated percentage of possible error associated with

diatom counting or chance alone; see Wolfe, 1997).

To examine trends over a relatively wide geographic

range, we compared several regional datasets that used

a technique known as the ‘top-bottom’ or ‘before and

after’ paleolimnological approach, which has been suc-

cessfully used to explore a large variety of environmen-

tal change issues (Smol, 2008). In brief, this approach

compares environmental indicators from discrete sedi-

mentary layers [top sediments: modern environment,

and bottom sediments: preindustrial environment

(before AD 1850)]. These broad-scale studies were in-

cluded in our analysis to provide additional data to

support our collection of detailed sediment core ana-

lyses, thereby adding to the geographic extent and

reproducibility of the taxon-specific trend within a

given region under examination. We acknowledge that

the depth in the core of the bottom sample varies from

lake to lake, as does the depth at which baseline (pre-

industrial) conditions would be reached. However, each

regional dataset used in this paper consists of several210Pb-dated and fully analyzed (whole core) sedimen-

tary profiles that serve to substantiate that the bottom

sediments represent preindustrial (pre-1850) diatom

assemblages (Smol, 2008) for each region. For example,

based on numerous dated cores, sediments from tem-

perate North American lakes deposited below 20–30 cm

typically represent pre-1850 lake conditions (e.g. Forrest

et al., 2002; Harris et al., 2006; Smol, 2008; as well as the

discussions in the original papers we cite).

For the ‘top-bottom’ portion of our synthesis, we have

collected the results of studies from the Northwest

Territories and Nunavut (Ruhland et al., 2003), from

New Brunswick (Harris et al., 2006), and from Ontario.

The Ontario lake-set consists of three separate studies

that we have combined into one representation of

Ontario [South-central Ontario: collected 1992 (Hall

& Smol, 1996); South-eastern Ontario: collected 1998

(Reavie et al., 2002); South-western Ontario: collected

1999 (Werner, 2003)]. To test whether the mean relative

abundances of diatom species (i.e. Cyclotella, Fragilaria,

Aulacoseira species) in the recent samples were signifi-

cantly different from the preindustrial sediment sam-

ples, we used a nonparametric Wilcoxon Signed-Rank

test for each regional lake set.

Detailed paleolimnological case study

To explore the primary mechanisms influencing the

plankton increases, we analyzed a high-resolution fossil

diatom record from Whitefish Bay, Lake of the Woods,

Canada (49.381N, 94.141W), in conjunction with long-

term climate-related instrumental and historical data.

Lakes in northwestern Ontario, such as Whitefish Bay in

the Lake of the Woods, are of particular interest as most

have remained relatively isolated from long-term influ-

ences of direct human perturbations and are often

considered ‘reference’ sites for local and regional im-

pact studies (e.g. ELA; Schindler, 1997). In addition,

climate records from northwestern Ontario have re-

ported some of the highest rates of temperature in-

creases in North America over the last few decades,

particularly during the winter (Schindler, 1997; Chiotti

& Lavender, 2008). Winter and spring snow fall has

decreased significantly in this region with significant

declines in streamflow since the 1970s (Chiotti & Laven-

der, 2008; Warren & Egginton, 2008). Although total

annual precipitation has increased, it is likely insufficient

to compensate for the rise in evaporation rates due to

substantially warmer temperatures (Schindler, 1997;

Warren & Egginton, 2008).

From a paleolimnological perspective, the exception-

ally high temporal resolution of the Whitefish Bay

sedimentary profile, the availability of long-term con-

tinuous climate data from the nearby town of Kenora,

and the existence of a rare long-term lake ice record

from this same site (Whitefish Bay) provided us with an

ideal opportunity to directly examine relationships

between diatom compositional changes and climate-

related instrumental and historical data. In addition,

to test the possibility that atmospheric nitrogen deposi-

tion may also have contributed to the recent increases in

planktonic Cyclotella taxa, we examined the relationship

between long-term nitrogen deposition data available

from Lake 239 in nearby ELA and our Whitefish Bay

diatom data. An examination of these relationships

seeks to provide insights into some of the plausible

triggers for this recent taxon-specific shift.

Kenora climate records dating back to 1899 were

attained from the Historical Adjusted Climate Database

for Canada available at the Environment Canada web-

site (http://www.cccma.ec.gc.ca/hccd/). We examined

monthly, seasonal, and annual temperature trends. The

continuous Whitefish Bay Lake ice record (starting in



1964) was obtained from the Ontario Ministry of Nat-

ural Resources, Kenora, Ontario, Canada. We examined

changes in the day in which ice formed on the lake (ice-

on), the day in which ice left the lake (ice-out), as well as

the number of ice-free days (ice-on day of year minus

ice-out day of same year – in Julian days). Atmospheric

inorganic nitrogen deposition data from 1970 to 2004

was collected at Lake 239 in the ELA and was measured

as total annual delivery in precipitation to the lake

surface (mg N m�2) (data provided by Department of

Fisheries and Oceans, Canada). Given the proximity of

Lake 239 to Whitefish Bay (�40 km), similar nitrogen

deposition rates are expected. Comparisons were made

between each of these measured datasets and trends in

the percent relative abundances of Cyclotella and Aula-

coseira species. Running means were applied to the

monitoring data, where appropriate, to ensure that

these data were compared to the diatom data at a

similar chronological interval.

Results

Meta-analysis: geographic extent of Cyclotella trend

Our meta-analysis included detailed diatom profiles

from 170 lakes that contained at least 2% relative

abundance of Cyclotella taxa in their sediments (Appen-

dix S2). Twenty-six of these lakes (15%) did not have

established chronologies (e.g. 210Pb dates) for the recent

sediments and thus could not be included in our

analysis. The remaining 144 diatom profiles met our

first two criteria, of which 41 lakes showed a decrease in

the relative abundance of Cyclotella species in the recent

sediments. However, closer inspection revealed that

95% of the profiles that reported decreases in Cyclotella

species were from lakes that had undergone cultural

eutrophication or acidification in their recent history

(e.g. Ek & Korsman, 2001; Lotter, 2001), and thus failed

our third criterion. Therefore, 105 lakes met our first

three criteria of which 84 lakes (80%) showed a 45%

increase in the relative abundance of Cyclotella species

since the mid-19th century (Fig. 1), 19 lakes (18%) did

not register an increase above 5% relative abundance,

and two lakes (2%) showed a decrease (Appendix S2).

Studies recording recent increases in Cyclotella species

were almost exclusively found in naturally occurring,

freshwater lakes from northern parts of North America

(i.e. Canada and the northern USA) and western Europe,

including both temperate and Arctic/alpine regions.

Notably, increases in small Cyclotella taxa were commonly

found in relatively pristine, nutrient-poor, nonacidified

lakes (e.g. lakes that have averted, or recovered from, the

effects of cultural eutrophication and acidification). An

interesting result that became evident from our meta-

analysis of studies containing diatoms from the species

Cyclotella was the identification of gaps in the geographi-

cal distribution of paleolimnological research. In some

parts of the Northern Hemisphere and in most of the

Southern Hemisphere, there was a distinct lack of paleo-

limnological records focusing on recent sediments (with

or without Cyclotella). For example, large sections of

Russia (particularly Siberia) and Northern Eurasia re-

main largely unsampled for diatom-based paleolimno-

logical analyses spanning the recent sediments

(MacDonald et al., 2004) Perhaps, not surprisingly,

much of the Southern Hemisphere did not yield paleo-

limnological studies suitable for the purposes of this

study, primarily because naturally occurring freshwater

lakes are not always abundant, human-made reservoirs

are common, and nonimpacted lakes are generally rare.

A comparison of general trends in the timing of initial

increases in Cyclotella species among the various bior-

egions (e.g. high latitude, high altitude and low lati-

tude) clearly demonstrated that high latitude sites,

although variable, recorded significantly earlier in-

creases than low latitude sites (Fig. 2a–c; ANOVA on

ranks, H 5 15.002, Po0.001, df 5 2). The median years

of change for high and low latitude sites were AD 1870

and 1970, respectively. The median age at which these

changes occurred in high altitude sites (located both in

temperate and in northern latitudes) was AD 1920. The

least amount of variability in timing was recorded in

temperate lakes, with 75% of the changes occurring

post-1940 (Fig. 2b).

Although the results from our detailed, dated cores

provided us with a large number of lakes (just under

100) that registered strikingly similar directional taxon-

specific diatom shifts, the addition of several regional

(i.e. top-bottom) diatom analyses gave us a more geo-

graphically extensive survey of the reproducibility of

this trend within a given region. Similar to the detailed

diatom profiles, top-bottom studies throughout Canada

(see Fig. 1 for locations) recorded statistically significant

(Po0.01; Wilcoxon Signed-Rank test) taxon-specific

changes in 120 out of 147 lakes (Fig. 3). Lakes from both

the Canadian subarctic and from temperate regions of

Canada, including New Brunswick and Ontario, showed

similar, clear patterns of increasing Cyclotella species (Fig.

3a, c and e). Concurrent with these planktonic increases,

small, benthic Fragilaria species, commonly found in lakes

with short open-water seasons throughout circumpolar

regions (Lotter & Bigler, 2000; Smith, 2002), recorded

higher relative abundances in the preindustrial sediments

of the subarctic lakeset (Fig. 3b), whereas heavily silicified

Aulacoseira species were more commonly found at higher

relative abundances in the preindustrial sediments of

temperate lakes (Fig. 3d and f). However, both Fragilaria

and Aulacoseira taxa were common to all latitudes.



Detailed paleolimnological case study

The Whitefish Bay diatom record from the Lake of the

Woods, Ontario (Fig. 4) shows a clear increase in small

planktonic Cyclotella species beginning ca. AD 1980 with

concurrent decreases in Aulacoseira subarctica (Fig. 1,

inset). This marked diatom floristic change closely

tracks an equally sharp rise in temperature recorded

at the Kenora climate station over the same time period

(Fig. 5a and b). A strong and significant positive corre-

Fig. 1 Geographical distribution of diatom-based paleolimnological studies that record an increase in the relative abundances of

planktonic Cyclotella species since the 19th century. Circles represent dated sediment cores where detailed diatom analyses have been

undertaken. Selected examples of these diatom stratigraphies are provided by the inset figures, which typify both the characteristics and

the timing of this trend for Arctic/alpine regions and for temperate lakes. Regional-scale coring sites [i.e. top-bottom or before–after

paleolimnological approach (Smol, 2008)] that record an increase in Cyclotella species in the modern sediments are represented by

squares. (A) Northwest Territories and Nunavut, Canada, n 5 40 (Ruhland et al., 2003), (B) Ontario, Canada, combined datasets, n 5 91

(Hall & Smol, 1996; Reavie et al., 2002; Werner, 2003), and (C) New Brunswick, Canada, n 5 16 (Harris et al., 2006).



lation was observed between Cyclotella relative abun-

dances and Kenora annual temperature data (r 5 0.73,

Po0.001), as well as a strong and significant negative

correlation between Aulacoseira abundances and annual

temperature trends (r 5�0.65, Po0.001).

Lake-ice records reveal that the ice-free period on

Whitefish Bay has lengthened by 28 days since 1964

(Fig. 6) and is, not surprisingly, strongly related to

increases in annual temperature recorded during this

period at the Kenora climate station (r 5 0.77, Po0.001).

The ice-out data show a strong inverse relationship to

increases in Cyclotella taxa (r 5�0.57, P 5 0.003) (Fig.

7a), and equally striking positive relationship to de-

creases in Aulacoseira taxa (r 5 0.66, Po0.001) (Fig. 7b).

Trends in long-term inorganic nitrogen deposition in

Lake 239 (ELA) revealed no significant relationship to

our taxon-specific diatom trends. We found that total

inorganic nitrogen deposition (TIN 5 NH4 1 NO3,

mg m�2 yr�1) at ELA was not significantly correlated to

Cyclotella (r 5 0.28, P 5 0.20) or to Aulacoseira (r 5�0.28,

P 5 0.20) relative abundance data in Whitefish Bay.

Discussion

The compilation of detailed diatom biostratigraphies

throughout the Northern Hemisphere (Fig. 1), supple-

mented with regional paleolimnological (i.e. ‘top-

bottom’) studies from various parts of Canada (Fig. 3),

shows a strikingly coherent, yet geographically asyn-

chronous large-scale pattern of ecological change. These

data indicate that extensive reorganizations of algal

community structure are evident in lakes across the

Northern Hemisphere since the mid-19th century. Spe-

cifically, abrupt increases in planktonic Cyclotella spe-

cies and concomitant decreases in heavily silicified

Aulacoseira and/or small, benthic Fragilaria species are

evident in regions where pronounced warming has

been recorded (e.g. Chapman & Walsh, 1993).

The onset of the shift to higher relative abundances of

Cyclotella taxa in Arctic lakes occurred significantly

(Po0.05) earlier (ca. AD 1870) than in lakes from tem-

perate latitudes (ca. 1970) (Fig. 2c). The higher varia-

bility in the timing of this shift among high latitude

lakes may be explained by the generally lower temporal

resolution of Arctic sediment cores, and differences in

the relative sensitivity of subarctic and high Arctic

lakes, both of which were grouped together in this

category. High altitude lakes, regardless of latitude

(Arctic–subarctic–temperate), were intermediate in

terms of the timing of this species change (ca. AD

1920). Despite the larger number of diatom profiles

collected from temperate lakes than from high latitude/

high altitude lakes for this meta-analysis, and large

differences in lake characteristics across the temperate

Northern Hemisphere, there was remarkable consis-

tency in the timing of Cyclotella increases recorded in

the biostratigraphic profiles from temperate lakes (i.e.

low variance) with 75% of these studies recording this

shift post-1940.

Cyc

lote

lla r

elat

ive

abun

danc

e (%

)

0

10

20

30

40

50

60 Whitefish Bay Emmett LakeWolfe LakeFairy Lake Indian LakeBig Rideau Lake

Year

1630

0

10

20

30

40

50Slipper LakeLake SaanajarviLake TK20Lake TK54Lake BirgervatnetLake CF-11

(a)

(b)

(c)

187

0

197

0

n = 60n = 7n = 15

High latitude

Yea

r

1750

1800

1850

1900

1950

2000

1870

19201970

1980193018801830178017301680

TemperateHigh altitude

Fig. 2 Comparison between the timing of the onset of planktonic

diatom increases showing the percentage relative abundances of

Cyclotella taxa in a selection of lakes from (a) high latitude and (b)

temperate regions. The median age of change is illustrated as a

straight line. Slipper Lake and Lake TK-20 (Ruhland, 2001); Lake

TK-54 (Paul, 2005); Lake Saanajarvi (from Sorvari et al., 2002); Lake

Birgervatnet (Jones & Birks, 2004); Lake CF-11 (Wolfe et al., 2006);

Emmett Lake (Werner et al., 2005); Wolfe Lake (Harris et al., 2006);

Fairy Lake (Quinlan et al., 2008); Indian and Big Rideau lakes

(Forrest et al., 2002). The trends portrayed in parts (a) and (b)

consist of combining small Cyclotella taxa, mainly C. stelligera,

C. pseudostelligera, C. glomerata, C. comensis, and C. gordonensis. (c)

A comparison in the timing of Cyclotella increases among different

bioregions (i.e. high latitude, high altitude, temperate) from

detailed diatom profiles collected in this meta-analysis. The earlier

timing of high latitude sites (median AD 1870) was significantly

different (Po0.05) than low latitude sites (median AD 1970):

ANOVA on rank; H 5 15.002; Po0.001; df 5 2. The timing of change

in high-altitude sites (median AD 1920) was not significantly

different from either high or low latitude lakes.



Preindustrial sedimentary diatoms

Mo

der

n s

edim

enta

ry d

iato

ms

Northwest Territories–Nunavut regional dataset (n=40)

% Cyclotella species0

% C

yclo

tella

spe

cies

0

10

20

30

40

50

60

70

% Fragilaria species

0

% F

ragi

laria

spe

cies

0

20

40

60

80

100

% Cyclotella species

0

% C

yclo

tella

spe

cies

0

10

20

30

40

50

60

70

% Aulacoseira species

0

% A

ulac

osei

ra s

peci

es

0

10

20

30

40

50

60New Brunswick regional dataset (n=16)

1:1

1:1

1:1 1:1

(a)

(c)

(e) (f)

(d)

(b)

% Cyclotella species

0

% C

yclo

tella

spe

cies

0

20

40

60

80

100Ontario combined regional datasets (n = 91)

% Aulacoseira species0

% A

ulac

osei

ra s

peci

es

0

20

40

60

80

1:11:1

P<0.010 P<0.012

P<0.003 P<0.011

P<0.001

P<0.001

70605040302010

10080604020 80604020

70605040302010 10080604020

605040302010

Fig. 3 The percent relative abundances of Cyclotella species, benthic Fragilaria species, and Aulacoseira species recorded in the top

sedimentary intervals (modern) vs. the bottom sedimentary intervals (pre-1850) for regional datasets from (a) Northwest Territories and

Nunavut in the Canadian subarctic, (Ruhland et al., 2003), (b) New Brunswick, Canada, (Harris et al., 2006), and (c) combined datasets

from Ontario including south-western Ontario, (Werner, 2003), south-central Ontario, (Hall & Smol, 1996), and south-eastern Ontario,

(Reavie et al., 2002). All lakes in figure had a total phosphorus (TP) measurement o20mg L�1 and/or did not record an increase in

diatom-inferred TP. Changes between the diatoms preserved in modern (top intervals) and preindustrial (bottom intervals) for each

lakeset were deemed significant using a Wilcoxon Signed-Rank test. P-values indicate significance after correcting for the False Discovery

Rate (Benjamini & Hochberg, 1995).



The response of aquatic organisms to climatically

induced changes is typically abrupt and pronounced

in the paleolimnological record when an ecological

threshold is exceeded. Such a regime shift has been

clear in high-latitude aquatic environments where a

sharp increase in species turnover was reported among

circumpolar lakes over the last ca. 200 years (Smol et al.,

2005). Most of the Arctic and alpine sedimentary pro-

files we present in Fig. 1 (e.g. Catalan et al., 2002; Sorvari

et al., 2002; Ruhland & Smol, 2005; Karst-Riddoch et al.,

2005) consist of diatom assemblages that have been

relatively stable for millennia with the most pro-

nounced changes starting in the 19th century. In all

these studies, a marked and unprecedented shift to a

diatom assemblage that is characterized by increases in

the relative abundances of planktonic Cyclotella species

suggests an abrupt transformation of aquatic habitat

availability and quality.

In comparison to the well-documented sensitivity of

high latitude/altitude environments to even moderate

changes in climate, freshwater ecosystems in more

southern (temperate) latitudes that experience longer

ice-free periods and growing seasons will, understand-

ably, take longer and/or require a greater increase in

temperature before passing through climate-related

ecological thresholds. This is consistent with the find-

ings from our meta-analysis where the median age of

increasing Cyclotella abundances recorded in temperate

lakes (ca. AD 1970) lagged this same taxonomic shift in

Arctic lakes by �100 years (Fig. 2a–c). The timing of

this change in temperate lakes of the Northern Hemi-

sphere is concurrent with instrumental records that

show a rise in air temperature post-1950 that is unpre-

cedented in the last millennium (Jansen et al., 2007).

The nature and timing of the recent diatom changes

recorded in our meta-analysis is consistent with warm-

ing that is associated with a shorter ice-cover period, a

longer diatom growing season, changes in the aquatic

light regime, increased nutrient cycling, and/or

changes to the thermal and mixing properties of lakes.

Changes in these lake water properties may provide

favorable habitats for small, fast-growing planktonic

Cyclotella species (Raubitschek et al., 1999; Rautio et al.,

2000; Pannard et al., 2008). C. stelligera and C. comensis

complexes, in particular, may exploit longer ice-free

periods and/or deeper, subsurface habitats where nu-

trient concentrations are somewhat elevated and where

light properties become more stabilized as thermal

stratification develops (Fahnenstiel & Glime, 1983).

For example, results from seasonal empirical studies

suggest that, after the onset of thermal stratification,

Cyclotella taxa (C. comensis, C. stelligera/pseudostelligera/

glomerata) may bloom in the metalimnion (the layer

of water below the mixed upper layer) where the

–96° –95° –94° –93°

49°

50°

Man

itoba

Ontario

Minnesota

Whitefish Bay

KenoraLake 239

0 10

km

–95°

45°

50°

55°M

a ni t

o

ba

Ontario

Minnesota

Man

itoba

–75°–80°–85°–90°

Fig. 4 Location of Whitefish Bay (Lake of the Woods, Ontario, Canada) showing the relative location of the Kenora climate station and

nearby Lake 239 in the Experimental Lakes Area (ELA).



temperature gradient is steepest (Fahnenstiel & Glime,

1983; Raubitschek et al., 1999), and are the dominant

taxa when the growing season is lengthened, spring

overturn period is extended, hypolimnetic waters are

warmer, and/or when water stability is at its peak

during autumn (Rautio et al., 2000). In contrast, earlier

sedimentary intervals from Arctic/alpine and temperate

profiles were dominated by diatoms with life strategies

linked to longer ice cover and/or greater turbulence. For

example, large, thickly silicified diatoms, such as Aula-

coseira taxa, require periods of resuspension through

turbulence to maintain their position in the water col-

umn (Kilham et al., 1996), and thus commonly decrease

in abundance during periods of strong stratification

(Pannard et al., 2008). During colder periods with ex-

tended ice cover (particularly in high latitude/altitude

lakes), opportunistic and pioneering diatoms, such as

small, benthic Fragilaria species, appear to be more

competitive (Lotter & Bigler, 2000), whereas planktonic

Cyclotella species fare poorly as extended ice cover

inhibits growth in the planktonic zone.

Tem

pera

ture

(°C

)

1.0

1.5

2.0

2.5

3.0

3.5

4.0

0

10

20

30

40

(b) Aulacoseira spp.

Date (year )

19001.0

1.5

2.0

2.5

3.0

3.5

4.0

% r

elat

ive

abun

danc

e

20

30

40

50

(a) Cyclotella spp.

1980–2002 mean annual temperature

r = 0.73, P<0.001

r = –0.65, P<0.001

2000199019801970196019501940193019201910

Fig. 5 Comparison of temperature data [Kenora (Ontario,

Canada) climate station] and diatom percent relative abundance

for Whitefish Bay (Lake of the Woods, ON, Canada). (a) Mean

annual temperature vs. Cyclotella species, (b) mean annual

temperature vs. Aulacoseira species. A 7-year running mean

was applied to the 100-year temperature record to enable com-

parisons to the diatom data. The Kenora temperature data is

available from http://www.ccma.bc.ec.gc.ca/hccd.

Year1960 1990

# of

ice-

free

day

s

180

190

200

210

220

230

240

250

260

Tem

pera

ture

(°C

)

0

1

2

3

4

5

6

# of ice-free daysAnnual temperature

y = 0.6556x + 203.64

r = 0.77

19801970 20102000

Fig. 6 Change in the number of ice-free days since 1964 from

the lake ice record from Whitefish Bay (Lake of the Woods,

Ontario, Canada). The number of ice-free days has increased

by � 28 days over the last four decades and is highly correlated

to the warming trend recorded at the Kenora (Ontario) climate

station for this same time period (Po0.001).

0

10

20

30

40

Ice-

out d

ay o

f yea

r

110

115

120

125

130

135

(b) Aulacoseira spp.

Date (year )

1965

% r

elat

ive

abun

danc

e

20

30

40

50

110

115

120

125

130

135

(a) Cyclotella spp.

r = –0.57, P = 0.003

r = 0.66, P<0.001

20052000199519901985198019751970

Fig. 7 Comparison of historical ice-out records and diatom

percent relative abundance for Whitefish Bay (Lake of the

Woods, Ontario, Canada). (a) Day of ice-out vs. Cyclotella species,

and (b) day of ice-out vs. Aulacoseira species. A 3-year running

mean was applied to the 35-year ice-out record to enable

comparisons to the diatom data. The Whitefish Bay ice-out data

was provided by the Ministry of Natural Resources, Kenora,

Ontario, Canada.



In general, the results of our meta-analysis indicate

that increases in small Cyclotella species were commonly

found in relatively pristine, nutrient-poor, nonacidified

lakes. This is consistent with previous studies that have

found Cyclotella species to be notably absent from lakes

that were directly impacted by anthropogenic activity,

such as acids from industrial emissions (Battarbee et al.,

1999), nutrients from agricultural and sewage runoff

(Stoermer et al., 1985), metal toxicity from industrial

effluents (Ruggiu et al., 1998), and the overdevelopment

of shorelines (Little et al., 2000). Understandably, cli-

mate-related changes in temperate regions may be

masked by direct anthropogenic stressors acting simul-

taneously on freshwater ecosystems. Therefore, in tem-

perate regions, reliable test sites for this climate-related

threshold response would logically be lakes that have

been minimally impacted by direct human disturbance

and/or other major stressors (e.g. eutrophication, acid

deposition) (Schindler, 1997). Our detailed case study

location, Whitefish Bay in the Lake of the Woods

(Fig. 4), provides such a setting.

The sharp increase in the relative abundance of

Cyclotella taxa and concurrent decrease in Aulacoseira

taxa recorded in our detailed analysis of the Whitefish

Bay sediment core (inset Fig. 1) are very similar in

nature (although asynchronous, as expected) to diatom

changes reported in both temperate (e.g. Fritz et al.,

1993; Alefs & Muller, 1999; Marchetto et al., 2004; Harris

et al., 2006) and circumpolar and alpine (e.g. Catalan

et al., 2002; Sorvari et al., 2002; Ruhland et al., 2003)

regions of the Northern Hemisphere. The striking re-

lationships observed between the Whitefish Bay diatom

data and the Kenora temperature record (both visually

and statistically) provide strong evidence that warming

trends over the past few decades have played an

important role in observed shifts in diatom community

structure (Fig. 5a and b).

A decrease in the duration of ice cover with warmer

temperatures, and associated changes in lakewater

properties, have often been surmised as triggering the

recent increases in planktonic Cyclotella species in sub-

arctic/alpine lakes (e.g. Lotter & Bigler, 2000; Catalan

et al., 2002; Sorvari et al., 2002; Ruhland et al., 2003;

Forsstrom et al., 2005; Smol et al., 2005). It follows that

long-term ice cover records could provide an ideal

means of verifying the relationship between recent

warming and increases in planktonic diatoms. For ex-

ample, a rare, long-term ice cover record available from

a river in Finland was used to indirectly corroborate

recent changes in diatom assemblage composition re-

corded in several neighboring lakes (Sorvari et al., 2002).

However, testing direct linkages between lake ice-cover

duration and these taxon-specific changes (i.e. changes

in the relative abundances of Cyclotella and Aulacoseira/

Fragilaria taxa) has not, as of yet, been undertaken,

understandably because continuous ice-out data for

the same lakes where diatoms have been examined

are extremely rare, particularly in remote Arctic and

alpine regions.

An increase in the ice-free period by almost 30 days

over the past ca. 40 years on Whitefish Bay is substantial

and has undoubtedly played a critical role in determin-

ing the structure and distribution of plankton commu-

nities throughout the water column. For example, the

strong and highly significant correlations between

Whitefish Bay ice-out and diatom trends (Fig. 7a and

b) suggest that recent increases in planktonic Cyclotella

taxa (decreases in Aulacoseira taxa) are predominantly

triggered by the lengthening of the ice-free period and

related changes in lakewater properties. These White-

fish Bay data corroborate the premise that abrupt in-

creases in Cyclotella species, concurrent with decreases

in Aulacoseira and Fragilaria species reported through-

out the Northern Hemisphere, can be primarily ex-

plained by climatically driven changes in lakewater

properties. In particular, these taxon-specific diatom

shifts were likely triggered by a warmer climate that

commenced in the mid-1800s, and escalated to unpre-

cedented highs over the last half century.

Other potential stressors and synergistic effects

The shift to planktonic diatom species, which we show

is correlated with recent warming in temperate lakes,

partly overlaps with a period of accelerated atmo-

spheric deposition of anthropogenically derived con-

taminants and nutrients. Increased deposition of

inorganic nitrogen, for example, has been cited as a

possible trigger for these abrupt compositional turn-

overs (e.g. Stoermer et al., 1985; Fritz et al., 1993; Wolfe

et al., 2003). However, we found no significant relation-

ship between inorganic nitrogen deposition from near-

by ELA and our diatom trends from Whitefish Bay. In

fact, Cyclotella relative abundance and ice-out data from

Whitefish Bay over this same time frame (i.e. 1974–2004)

were significantly and negatively correlated (r 5�0.45,

P 5 0.03), adding further support that climate-related

factors are primarily responsible for recent taxon-

specific diatom shifts. The relationships found in our

case study are consistent with findings in nearby

regions. For example, recent increases in the relative

abundance of Cyclotella species have been reported in

lakes in south-central Ontario since the early 1980s

(Clerk et al., 2000; Quinlan et al., 2008) where significant

increases in the duration of the ice-free period have

been recorded in these lakes since the mid-1970s (Futter,

2003). However, no statistically significant trend has



been noted in nitrate or ammonium deposition over the

past three decades (Schindler et al., 2006).

The lack of a strong relationship between recent

diatom community reorganization and nitrogen deposi-

tion in our case study is also consistent with recent

paleolimnological findings in the Arctic (Smol &

Douglas, 2007; Keatley et al., 2008) where the effects of

climatic change are first experienced. Aerially trans-

ported nutrients and contaminants would reach Arctic

and alpine lakes decades after these pollutants would

reach temperate lakes; however, the changes in diatom

species occur decades earlier in the former. Therefore,

the timing of these taxon-specific diatom shifts predat-

ing the onset of anthropogenic pollutants in Arctic lakes

underscore that aerially transported nutrients and/or

contaminants cannot explain the marked hemispheric-

scale diatom shifts we describe.

Although we have found no support to link increases

in Cyclotella species to nitrogen deposition, it is pos-

sible that a rise in inorganic nitrogen deposition may

be linked to recent climatic changes. For example,

in regions proximal to nitrogen sources, changes in

precipitation could be important for the delivery of

atmospheric inorganic nitrogen to nearby lakes (Macdo-

nald, 2005). A comparison of Kenora precipitation data

with the ELA TIN data resulted in an nonsignificant

positive correlation (r 5 0.33, P 5 0.06). Although not

conclusive, the possibility of a synergistic relationship

exists. While it is clear that diatoms respond to a multi-

tude of complex factors, it is equally clear that the nature,

magnitude, and timing of these taxon-specific diatom

shifts are best explained by recent warming and asso-

ciated limnological changes.

Conclusions

The diatom data included in our meta-analysis of over

200 lakes provide a spatially coherent picture that

climate-driven, taxon-specific changes are now evident

across vast regions of the Northern Hemisphere repre-

senting a wide spectrum of lake ecosystems. Although

the degree of ecological change may vary between lakes

(as would be expected, based on morphometry and

other limnological variables), the similarity in this dia-

tom trend across a regional scale is striking. Freshwater

ecosystems in the Northern Hemisphere have crossed

ecological thresholds with changing climate that

were initiated in the 19th century in Arctic and alpine

regions, but typically only occurred in the mid-20th

century in lakes from mid-latitude regions of North

America and western Europe. The recurring and wide-

spread trend of recent increases in the relative abun-

dances of planktonic Cyclotella species is strongly

correlated to recent increases in temperature and sub-

stantially longer ice-free periods. Synergistic effects

between climate warming and other human-induced

stressors also occur (Wolfe et al., 2006). However, based

on the timing, magnitude, and nature of the diatom

changes, we conclude that climatically induced change

in lake-ice cover (and associated limnological changes)

was the primary explanatory metric for hemispheric-

scale increases in planktonic Cyclotella species over the

last ca. 200 years. Our findings are particularly trou-

bling given that the ecological changes we report are

widespread, and have occurred with increases in mean

annual temperatures that are substantially lower than

levels projected by climate models for both high- and

mid-latitude regions of the Northern Hemisphere. If

this rate and magnitude of temperature increase con-

tinues, it is likely that new ecological thresholds will be

crossed, many of which may be unexpected.

Acknowledgements

We thank R. Hall, A. Harris, E. Reavie, and P. Werner for kindlyallowing the use of their data for producing Fig. 3, M. Stainton(Department of Fisheries and Oceans, Canada) for providing thesediments and dating the Whitefish Bay core, the Lake of theWoods District Property Owners Association for supporting fieldwork for the Whitefish Bay core, and M. Turner (Department ofFisheries and Oceans, Canada) for providing nitrogen depositiondata from ELA. We thank two anonymous reviewers for theirthoughtful and constructive comments that helped to strengthenand clarify this paper. This work was supported by the NaturalSciences and Engineering Research Council of Canada (to J. P.Smol), and the Ministry of the Environment, Ontario.

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Supplementary material

The following supplementary material for this article is avail-

able online:

Appendix S1. List of diatom taxa including taxonomic

authorities, taxonomic synonyms, and the species complexes

referred to in manuscript.

Appendix S2. Results of literature search for paleolimnological

studies containing Cyclotella species. Lake names in bold

indicate studies with suitable chronology and that reported

increases in Cyclotella species 45%. Rows shaded in grey

indicate all studies that did not have suitable chronology.

Studies without a suitable chronology but that had 45%

relative abundance of Cyclotella taxa (i.e. 12 studies)

were tallied in the chronology column. HL 5 high latitude;

HA 5 high altitude; T 5 temperate lakes are sorted by

author(s) in alphabetical order. Lakes in bold that had

suitable chronology and that showed 45% increase in the

relative abundance of Cyclotella taxa were plotted in Fig. 1.

In general, lakes considered to be unpolluted had total

phosphorus (TP) concentrations o20mg L�1 and pH46.0.

w/ 5 with; w/o 5 without; ON 5 Ontario; BC 5 British

Columbia; NW 5 Northwest; NS 5 Nova Scotia; NB 5 New

Brunswich; QC 5 Quebec; USA 5 United States of America.

This material is available as part of the online article from

http://www.blackwell-synergy.com/doi/abs/10.1111/

j.1365-2486.2008.01670.x

Please note: Blackwell Publishing is not responsible for the

content or functionality of any supplementary materials

supplied by the authors. Any queries (other than missing

material) should be directed to the corresponding author for

the article.



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