Oecologia (2001) 128:1–14
DOI 10.1007/s004420100655
Geir Ottersen · Benjamin Planque · Andrea Belgrano
Eric Post · Philip C. Reid · Nils C. Stenseth
Ecological effects of the North Atlantic Oscillation
Received: 25 July 2000 / Accepted: 5 January 2001 / Published online: 13 March 2001
© Springer-Verlag 2001
Abstract Climatic oscillations as reflected in atmospheric modes such as the North Atlantic Oscillation
(NAO) may be seen as a proxy for regulating forces in
aquatic and terrestrial ecosystems. Our review highlights
the variety of climate processes related to the NAO and
the diversity in the type of ecological responses that different biological groups can display. Available evidence
suggests that the NAO influences ecological dynamics in
both marine and terrestrial systems, and its effects may
be seen in variation at the individual, population and
community levels. The ecological responses to the NAO
encompass changes in timing of reproduction, population dynamics, abundance, spatial distribution and interspecific relationships such as competition and predatorG. Ottersen
Institute of Marine Research, P.O. Box 1870 Nordnes,
5024 Bergen, Norway
B. Planque
IFREMER, Laboratoire d'Ecologie Halieutique, BP 21105,
44311 Nantes, Cedex 03, France
A. Belgrano
Kristineberg Marine Research Station,
The Royal Swedish Academy of Sciences, 2130 Kristineberg,
450 34 Fiskebäckskil, Sweden
E. Post
208 Mueller Lab, Department of Biology, Penn State University,
University Park, PA 16802-5301, USA
P.C. Reid
Sir Alister Hardy Foundation for Ocean Science (SAHFOS),
1 Walker Terrace, Plymouth, PL1 3BN, UK
N.C. Stenseth (✉)
Division of Zoology, Department of Biology, University of Oslo,
P.O Box 1050 Blindern, 0316 Oslo, Norway
e-mail: n.c.stenseth@bio.uio.no
Fax: +47-22-854605
N.C. Stenseth
Flødevigen Marine Research Station,
Institute of Marine Research, 4817 His, Norway
Present address:
G. Ottersen, Division of Zoology, Department of Biology,
University of Oslo, P.O Box 1050 Blindern, 0316 Oslo, Norway
prey relationships. This indicates that local responses to
large-scale changes may be more subtle than previously
suggested. We propose that the NAO effects may be
classified as three types: direct, indirect and integrated.
Such a classification will help the design and interpretation of analyses attempting to relate ecological changes
to the NAO and, possibly, to climate in general.
Keywords North Atlantic Oscillation · Climate · Marine
ecosystem · Terrestrial ecosystem · Population ecology
Introduction
Individuals and populations undoubtedly experience climate locally, through temperature, wind, currents, rain
and snow. Nevertheless, such meteorological and oceanographic features are often governed by phenomena extending over much larger areas. Interaction between the
ocean and atmosphere may form dynamic systems, exhibiting complex patterns of variation, which profoundly
influence ecological processes in a number of ways. In
this review, we discuss such climatically mediated ecological effects.
The most well known example of a large-scale oceanatmosphere oscillating system is the El Niño-Southern
Oscillation (ENSO; Philander 1990) originating in the
tropical Pacific and generating impacts in both marine
and terrestrial environments over a large part of the
globe (Allan et al. 1996). In the North Atlantic there exists a climate system of a different nature, but with comparably extensive effects, namely the North Atlantic Oscillation (NAO). Considering that ecological systems are
generally non-linear (May 1986), even slight changes induced by fluctuations in large-scale climate phenomena
– like the NAO – may produce large effects at various
trophic levels (Post et al. 1999a).
The response to the NAO in surface air temperature
has been recognised since at least 1770 (Saabye 1776)
and scientists have been studying it since the 1880s (D.B.
Stephenson at http://www.met.rdg.ac.uk/cag/NAO/in-
2
dex.html). However, only fairly recently has the NAO
been revealed as a major driving force of the climatic systems of the northern hemisphere (van Loon and Rogers
1978; Rogers 1984; Hurrell 1995). Almost all the early
work on the NAO dealt solely with physical aspects.
Since the mid 1990s, an increasing number of investigations focusing on the relationships between the temporal
patterns seen in the NAO and the variability observed in
biological populations has appeared in the literature. D.B.
Stephenson (http://www.met.reg.ac.uk/cag/NAO/biblioall.html) lists a total of 183 articles over the period
1981–1999 using “North Atlantic Oscillation” in the title
or abstract. Of the 14 articles in this list linking the NAO
to ecology, 9 were published in 1999, 3 in 1995–1998 and
only 2 earlier, the first in 1993 (Downton and Miller
1993).
It thus seems timely to assess the possible influence
of the NAO on ecological processes and patterns in the
North Atlantic region by reviewing the available literature. In this overview, we summarise pertinent information regarding the atmospheric and oceanic characteristics of the NAO and assess the variability in ecological
response. Throughout, the NAO is considered a proxy
for a variety of climatic processes. We cover both
plants and animals, in marine as well as terrestrial systems. On this basis, we draw together the insights,
emerging for each of the reviewed systems, to an overall conclusion. As part of the concluding section, we
provide perspectives for future approaches to study the
mechanisms involved, linking climatic variability
(through proxies, such as the NAO) to ecological processes and patterns.
The NAO as a proxy
The climate scenario
The NAO is an alternation in the pressure difference between the subtropic atmospheric high-pressure zone centred over the Azores and the atmospheric low-pressure
zone over Iceland (Fig. 1). The NAO has a broad band
spectrum with no significant dominant periodicities (unlike the ENSO). More than 75% of the variance of the
NAO resides in shorter than decadal time scales (D.B.
Stephenson at http://www.met.rdg.ac.uk/cag/NAO/index.html). The NAO is globally one of the most robust
modes of recurrent atmospheric behaviour (Barnston and
Livezey 1987). It is the dominant mode of atmospheric
behaviour in the North Atlantic sector throughout the
year, but it is most pronounced during winter and accounts for more than one-third of the total variance in
sea level pressure (SLP) (Cayan 1992; Hurrell 1995).
Several indices for the NAO have been defined, notably
those by Rogers (1984) and extended further back in
time by Hurrell (1995) and Jones et al. (1997). Hurrell’s
winter (December through March) index of the NAO is,
for example, based on the difference in normalised SLPs
between Lisbon, Portugal, and Stykkisholmur, Iceland,
from 1864 through 1995. The SLP anomalies at each station were normalised by division of each seasonal pressure by the long-term (1864–1995) standard deviation.
A high or positive NAO index is characterised by an
intense Icelandic Low and a strong Azores High. The increased pressure difference results in more and stronger
winter storms crossing the Atlantic Ocean in a more
northerly track. The reduced pressure gradient of the
low-index or negative NAO phase leads, on the other
hand, to fewer and weaker winter storms crossing on a
more west-east pathway. Variability in the direction and
magnitude of the westerlies is responsible for interannual
and decadal fluctuations in wintertime temperatures and
the balance of precipitation and evaporation over land on
both sides of the Atlantic Ocean (Rogers 1984; Hurrell
1995). The relationship between the state of the NAO
and the temperature, wind and precipitation patterns is
particularly strong in northern Europe, for which the
NAO index is often a proxy (Fig. 1).
The scale of the influence of the NAO on long-term
variation in winter climate is most readily apparent from
the fact that between 1935 and 1994 it accounted for approximately half of the increase in winter temperature
throughout the extratropical northern hemisphere
(Hurrell and van Loon 1997). Regionally, nearly all of
the cooling in the north-west Atlantic and the warming
across Europe since 1980 may, furthermore, be linearly
related to changes in the NAO. The NAO is also seen to
influence the distribution and fluxes of major water
masses and currents in the Atlantic and to govern deep
water formation in the Greenland Sea and intermediate
water in the Labrador Sea (Dickson 1997; Curry et al.
1998; Reid et al. 1998a). The possible influence of the
NAO on the latitude of the Gulf Stream has been discussed by Taylor and Stephens (1998) and Taylor et al.
(1998). However, there is still uncertainty about the measurement of the Gulf Stream latitudinal position; hence
whether the NAO precedes the Gulf Stream oscillations
or if the two phenomena fluctuate in synchrony remains
unclear (Joyce et al. 2000).
Regional and temporal variability in the impact
of the NAO
Temperature plays an essential role in many ecological
mechanisms. Hence, the NAO may operate through temperature effects. However, the value of the NAO as a
proxy for sea or land temperature varies regionally and
must be evaluated when studying specific areas. This is
so on the full North Atlantic scale, regionally between
different European areas, and locally according to altitude on, for example, the Norwegian west coast (Mysterud et al. 2000).
A positive NAO phase is associated with strong wind
circulation in the North Atlantic, high atmospheric and
sea temperatures in western Europe and low temperatures on the east coast of Canada (Mann and Lazier
1991). An opposition in winter temperatures in Green-
3
Fig. 1 a Temporal development of the North Atlantic Oscillation (NAO) winter index as
defined by Jones et al. (1997)
over the last 170 years [red
(positive NAO) and blue (negative NAO) bars representing
annual values, black curve representing smoothed values].
b Positive NAO phase characterised by a pronounced difference in sea level pressure
(SLP) between the high-pressure zone around the Azores
(the Azores High) and lowpressure zone around Iceland
(the Iceland Low). During a
positive phase- the prevailing
westerly winds are strengthened causing increased precipitation and temperatures over
northern Europe and southeastern USA and dry anomalies
in the Mediterranean region
(from http://www.ldeo.columbia.edu/~cullen/images/NAO+phase.GIF). During a
negative phase (not shown), the
difference in SLP is smaller,
the westerlies weaker, temperatures decrease in northern Europe and increase in northern
Canada and Greenland. c The
distribution of the SLP field
during winter. d,e Correlation
between the NAO winter index
and winter sea surface temperature (SST) (d) and winter scalar
wind (e) for the period
1950–1995. SST and scalar
wind data are from the COADS
database (Woodruff et al. 1987)
land and western Europe was noted as far back as 1776
(Saabye 1776) and the inverse fluctuation in Barents and
Labrador Sea temperatures has also been known for
quite some time (Izhevskii 1964). The role of the NAO
in this “seesaw” pattern was explored by van Loon and
Rogers (1978). The NAO index accounts for approximately 50% of the interannual climate variability in both
the Labrador and Barents Sea regions (Drinkwater and
Myers 1997; G. Ottersen and N.C. Stenseth, unpublished
data), but with opposite effects.
The correlation between the NAO index and winter
sea surface temperature (SST) and wind strength varies
between European regions (Fig. 1). The NAO appears to
be a good proxy for winter SST and wind strength in the
North Sea, but this is certainly not so on the western
coast of the Iberian peninsula. The NAO is primarily a
winter phenomenon, so its connection with the wind,
temperature and precipitation fields is strongest during
winter. This suggests in the first instance that ecological
mechanisms operating during winter are more likely to
be affected by the NAO than those operating during
summer. However, whilst the connection between scalar
wind and the NAO is only perceptible during the winter
months, the link between the NAO and SST may carry
over through to the summer as sea temperature anomalies persist. Again, the persistence of temperature anomalies is region dependent and should be assessed for any
particular area (see for example Planque and Frédou
1999). As for temperature and wind, the correlation of
precipitation with the NAO varies between region (Dickson et al. 2000). The correlation fields of temperature,
wind and precipitation all meet on the Norwegian coast
4
where a high NAO is linked to stronger winds, higher
levels of precipitation and milder temperatures. This
strong regional correlation of the NAO with the three
major driving forces of weather variability can, to some
extent, explain the substantial evidence for an ecological
influence of the NAO reported in Norway.
Even within regions where the link between the NAO
and local climate is at its strongest, as along the Norwegian west coast, ecological responses to NAO fluctuation
may vary greatly at small spatial scales. Mysterud et al.
(2000) demonstrated that the correlation between snow
depth and the NAO is negative at low altitudes, but positive above 400 m.
The NAO and its ecological effects
Temperature-mediated responses
The most obvious and probably best-documented influence of the NAO on marine and terrestrial ecosystems is
through temperature. This is particularly evident in
north-western Europe where the NAO and temperature
are closely related, with high winter and spring temperatures during years of high NAO index and vice versa.
Because temperature affects the metabolic rates of species without thermal regulation (i.e. the large majority of
species), the effects are likely to be seen in most components of an ecosystem.
As a result of warming during winter-spring in the
past three to four decades, possibly related to increasingly positive NAO index values, the length of the active
growing season for terrestrial plants has increased in the
northern part of the northern hemisphere (Myneni et al.
1997), and particularly in Europe (Menzel and Fabian
1999). Similarly, the length of the growing season of
phytoplankton in the North Sea has increased in parallel
with the warming of SST associated with the NAO (Reid
et al. 1998a).
Higher temperatures may increase juvenile survival
rate and population density of birds in the UK (Slagsvold
1975), and furthermore influence the timing of reproduction of a number of terrestrial species in Europe,
such as UK amphibians and birds, which spawn or lay
eggs earlier in warmer years (Beebee 1995; Crick et al.
1997; McCleery and Perrins 1998; Crick and Sparks
1999). Forchhammer et al. (1998a) relate this consistent pattern of earlier breeding during a period of increasingly warm winters to the highly positive NAO
phase from 1970 to 1994. However, whether the change
in timing of reproduction described in these last examples is a direct consequence of a physiological response
to temperature, or if it reflects variability in the timing
of food availability in spring, as suggested by Visser et
al. (1998) in their study of bird populations in The
Netherlands, is unclear.
The increase in temperature and alteration in the winter circulation pattern observed during the last decades
of predominantly positive NAO index values have re-
Fig. 2 The relationship between the NAO index and two copepod
species in the northeast Atlantic: Calanus finmarchicus (a) and
C. helgolandicus (b). Regressions show the log abundance of each
species against the NAO index for the period 1958–1995. The
maps indicate the difference in log abundance between years of
high and low NAO. Crosses indicate a negative difference (i.e.
abundance lower during years of high NAO index)
sulted in unfavourable conditions for the population of
the copepod Calanus finmarchicus, leading to a significant decrease in the abundance of the species. Conversely, these hydroclimatic shifts have proved beneficial to
C. helgolandicus, the abundance of which has increased
during these years (Fromentin and Planque 1996;
Planque and Fromentin 1996; Fig. 2).
The effect of temperature on individual growth is
evident in, for example, the stock of Arcto-Norwegian
cod (Gadus morhua) with warm years (positive NAO)
favouring higher growth rates (Loeng et al. 1995;
Michalsen et al. 1998; Ottersen and Loeng 2000;
Fig. 3). The same is true in lower latitudes and is observed, for example, in the case of North Sea cod
(Brander 1995). A number of relationships between the
NAO and recruitment to marine fish populations have
been attributed to the effects of temperature. However,
temperature acts on almost every biological step leading to recruitment: adult growth (Brander 1995), adult
maturity (Tyler 1995), timing of spawning (Hutchings
and Myers 1994; Kjesbu 1994), egg viability (Flett et
al. 1996), timing of food availability (Ellertsen et al.
1989; Nakken 1994) and larval growth and mortality
(Pepin 1990; Otterlei et al. 1999). Consequently, mechanism(s) suggested to underlie the climate-fish recruitment links shown in a number of explorative studies remain fairly speculative.
5
Fig. 3 The link between the
NAO and recruitment to the
Arcto-Norwegian (Barents Sea)
cod stock (a) and suggested
mechanisms (b–d). b The NAO
index (December–March, from
Hurrell 1995) is positively correlated with Barents Sea annual
mean temperature as measured
along the Russian Kola meridian transect (Tereshchenko
1996) which is positively
linked to the mean length of 0group (5-month-old) cod measured in August (c) which
again is an indicator of abundance of the same cohort at later stages (abundance at age 3
shown) (d). c Adapted from
Loeng et al. (1995). d Adapted
from Ottersen and Loeng
(2000)
Some of the effects of the NAO may be carried by a
biological population over a number of years following
a particular NAO situation. For example, the increase
in survival through the vulnerable early stages of northerly cod stocks off Canada, West Greenland and Norway during warm years historically results in stronger
year-classes at later, catchable, stages (Ottersen 1996).
When the year-class matures, the number of spawners
as well as their individual size may be increased, enhancing the potential for high recruitment to the next
generation. Furthermore, if individuals in a cohort of
Arcto-Norwegian cod are larger than average as halfyear-olds, such a cohort tends also to be abundant when
the fish grow older (Ottersen and Loeng 2000; Fig. 3).
On the other hand, the year-class strength of cod in the
North and Irish Seas is inversely related to a positive
NAO phase and high temperature. This is possibly a result of limitation in energy resources necessary to
achieve higher metabolic rates during warm years
(Planque and Fox 1998). In both cases, the effects of
the NAO are perceived in the fisheries with a lag of
several years.
strongest in this area (Xie and Arkin 1996; Dickson et al.
2000). However, since temperatures in the region often
are around 0°C during winter (Mysterud et al. 2000), the
relationship between the NAO and snow depth is complex and debated. Post et al. (1999b) documented positive correlations between the NAO and snow depth and
thus argued that a high NAO index indicates severe winter conditions for red deer. This positive correlation was
based on meteorological data from a station located
above 400 m. Mysterud et al. (2000) found, however, a
negative correlation between the NAO and snow depth at
altitudes below 400 m, where the deer stay over the winter (Albon and Langvatn 1992).
The amount of snow in an area is also a critical determinant of the timing of onset of plant production in
spring. Warm and wet winters (i.e. a positive NAO) are
generally associated with earlier, more prolonged and
more spatially variable flowering across much of Norway (Post and Stenseth 1999). Disentangling the effects
of snow cover from those of temperature is, however,
difficult since the two abiotic factors are closely synchronised.
The NAO as a measure of winter severity
The influence of the NAO through regulating wind and
oceanic circulation
For northern ungulates, severe winters are those with
deep snow, imposing extreme energetic costs of foraging
and locomotion (Hobbs 1989; Parker et al. 1984). On the
western coast of Norway, the NAO is positively correlated with temperature and precipitation (Post et al. 1997).
The link between the NAO and precipitation is at its
The persistent anomalies in the wind field associated
with the NAO are responsible for alterations in the direction and strength of oceanic surface currents. Currents in
shallow areas are particularly influenced by variable
wind conditions. This is the case for the intensity of the
6
Fig. 4 Graphs of annual means
(modified from Reid et al., in
press) for a standardised plot of
the NAO (a), zooplankton (second principal component) for
the North Sea (b), sea surface
temperature for the North Sea
(c), horse mackerel catches
from the North Atlantic between 45° and 65° N (d), phytoplankton colour for the North
Sea (e) and modelled inflow into the North Sea (f)
flow of Atlantic water entering the North Sea. The abundance of C. finmarchicus in the North Sea is thought to
depend upon the quantity of individuals seeded from the
Faeroe-Shetland Channel at the end of winter (Heath et
al. 1999). Several authors have suggested that the NAOdriven changes in Atlantic inflow are, at least in part, responsible for the observed changes in C. finmarchicus
abundance in the northern North Sea (Planque and Taylor 1998; Stephens et al. 1998; Gallego et al. 1999;
Heath et al. 1999). Variations in the volume of Atlantic
water entering the North Sea have been associated with
changes in a variety of ecological groups, from phytoplankton to fish, and Reid et al. (in press) suggested the
dramatic change observed after 1987 may be part of a regime shift (Fig. 4).
Off northern Norway, the NAO affects the regional
wind field, which again influences the north-eastward
flow of warmer Atlantic water and ultimately the temperature of the Barents Sea (Ådlandsvik and Loeng
1991; Dickson et al. 2000). Helle and Pennington (1999)
have shown that in this region, the volume of inflow is
related to the abundance of zooplankton (primarily C.
finmarchicus) and that this effect is mediated through the
food web up to cod juveniles. Apart from the direct regional effect of the NAO on surface circulation, the
NAO affects large-scale convection activity in the North
Atlantic and is responsible for changes in the circulation
of surface and deep waters (Dickson 1997). These
changes can affect populations over much greater time
scales. The North Sea population of C. finmarchicus is,
as already mentioned, seeded from the Faeroe-Shetland
Channel where it overwinters in Norwegian Sea Deep
Water (NSDW). Changes in convective intensity over
the past decades have been associated with a decrease of
the volume of NSDW. Heath et al. (1999) proposed that
this reduction in the volume of C. finmarchicus-overwintering habitat is partly responsible for the long-term decline in abundance of the species observed in the North
Sea.
Effects on the spatial distribution of species
Alteration in the geography of weather patterns linked to
the NAO also seems to affect the spatial distribution of
species. Warming trends in Europe have, for example,
been related to changes in the geographical range of butterflies (Parmesan et al. 1999) and birds (Thomas and
Lennon 1999). The same was found in the ocean, where
the size of the thermal habitat of Atlantic Salmon (Salmo
7
salar) has fluctuated in parallel with changes in the NAO
(Friedland et al. 1998; Dickson and Turrell 1999), decreasing during the years of positive NAO and expanding during negative phases of the oscillation. Similarly,
the habitat range of cod in the Barents Sea expands into
the eastern and northern regions, which are normally too
cold for cod, during warmer periods related to a positive
NAO phase (Nakken and Raknes 1987; Ottersen et al.
1998).
Long catch records, some spanning several hundred
years, of herring (Clupea harengus) and sardines (Sardina pilchardus) from northern Europe (Alheit and Hagen
1997), show that the fisheries were intense in some periods and totally absent in others, and that these “fish periods” varied regionally. One group of stocks (for example
herring off the Swedish west coast and southern England) are favoured during periods with a negative value
of the NAO index when the westerly winds are shifted to
the south and the sea temperatures in the regions are low,
whereas another group (e.g. sardines in northern France
and southern England, and Norwegian spring-spawning
herring) benefit from the opposite regime. This pattern
of alternating periods may be explained as a response to
different regimes of prevailing wind directions corresponding to related NAO modes (Alheit and Hagen
1997).
Effects on predator-prey interactions
and between-species competition
Changes in climate patterns associated with the NAO
also affect predator-prey interactions. In the North Sea,
winter temperature appears to control the abundance of
the marine polychaete Nephtys hombergii and, through a
cascading effect, the abundance of the two smaller polychaete prey species Scoloplos arminger and Heteromastus filiformis (Beukema et al. 2000). In the Barents Sea,
the increase in basic metabolic rates of cod, associated
with a higher temperature during years of high NAO, can
result in a rise in the consumption of capelin (Mallotus
villosus) by 100,000 tonnes per degree centigrade
(Bogstad and Gjøsæter 1994). Furthermore, the variations in reproduction timing of birds and amphibians reported above are also thought to be partly operating via
trophic interactions.
Tunberg and Nelson (1998) suggested that the changes observed in the macrobenthic biomass along the
Swedish western coast are controlled by the level of primary production in the surface layer which is NAO dependent. A similar hypothesis was formulated by
Fromentin and Planque (1996) who suggested that the
fluctuations in the abundance of the copepod C. finmarchicus in the North Sea were partly due to NAOdriven changes in phytoplankton production. The influence of the NAO via trophic intermediates has also been
hypothesised for the Canadian lynx (Stenseth et al. 1999)
and Norwegian red deer (Forchhammer et al. 1998b;
Post and Stenseth 1999). In North America, dynamics
associated with the NAO also affect changes in abundance of moose (Alces alces), white-tailed deer (Odocoileus virginianus), and their primary predator, wolves
(Canis lupus) (Post and Stenseth 1998), as well as interactions between wolves and their prey (Post et al.
1999c). The latter is an example of how the NAO may
mediate ecosystem dynamics in relatively simple systems through effects on predators, which cascade down
onto secondary and primary producers.
In the case of bird populations (the flycatchers Ficedula hypoleuca and F. albicollis), comparable modulation of competition by NAO-related environmental
changes has been described by Sætre et al. (1999).
More complex responses to the NAO
Complex responses to the NAO generally involve a direct physiological response to some NAO-related environmental process followed by subsequent modulation
of population dynamics and/or competitive interactions,
and interactions between predator and prey species.
Such links are often non-linear (e.g. May 1986) and
therefore difficult to characterise. The link between climate variability and ecological processes may indeed be
viewed as an integrated part of the field of macroecology (Brown and Maurer 1989; Brown 1995, 1999;
Gaston and Blackburn 1999; Maurer 1999) in the sense
that climatic and environmental forcing need further
consideration in attempts to study ecologically complex
systems.
Such complex responses to the NAO have been described in a number of studies on plants and terrestrial
mammals in Norway and North America. Plants of
many terrestrial species bloom earlier by an average of
2–4 weeks following positive NAO (warm) winters
throughout much of Norway (Fig. 5a). This is the case
both in areas near the coast, that are typically snow free,
and in areas further inland that have a higher snowfall
during warm winters (Post and Stenseth 1999). An advance in plant phenology of this magnitude may be sufficient to profoundly increase the number and size of
seeds produced, as well as seedling survival (Schmitt
1983; Galen and Stanton 1991). Female red deer
(Cervus elaphus) born in positive NAO years apparently
benefit from earlier availability of these highly nutritious plants and may be as much as 25% more likely to
conceive as yearlings (Post and Stenseth 1999). The enhanced fecundity of female red deer born after positive
NAO winters in Norway contributes subsequently to increases in red deer abundance of 2 years later, when
they produce their first calves (Fig. 5c; Forchhammer et
al. 1998b). In fact, in several populations of red deer,
both in Norway (Forchhammer et al. 1998b) and on the
Isle of Rum in Scotland (Post et al. 1999a), delayed,
positive relationships between warm NAO winters and
abundance of red deer appear to be explained by enhanced female fecundity following years when the winter ends relatively early.
8
Discussion
Current interest in the ecological effects of the NAO will
likely generate a plethora of new investigations, which
may soon provide both new answers to old questions as
well as new questions. However, the range of current examples is sufficient to call for reflection on the ways in
which the NAO and biological populations may be
linked and how research in this field is presently conducted.
How many correlations can one meaningfully derive?
As seen from the many examples presented, correlation
analysis has remained the favoured method for the identification of NAO-ecology links. Almost every possible
type of correlation has been used: parametric or nonparametric, direct or lagged, on raw data or on transformed time-series (first-order differencing, removal of
trend and so on). Each method has distinct properties and
the results they produce should not be interpreted in the
same way. For example, lagged correlations suggest a
delay between the climate-forcing associated with the
NAO and the biological response. Significant correlations on detrended or differenced time-series indicate
that the ecological response to the NAO probably occurs
rapidly (within a year). On the other hand, correlations
that are significant on raw data but not on detrended series suggest a degree of inertia between the NAO signal
and the biological response. Recognising these differences is important as they often provide useful information for selecting plausible underlying mechanisms.
Being conservative regarding tests of statistical significance is also necessary. After computing 100 correlation coefficients, to find 1 that is significant at the 1%
level is, of course, not surprising. Since analyses showing non-significant correlations often find their way into
the wastepaper basket, however, one can often lose track
of this fact (Shepherd et al. 1984). A good remedy is to
apply an overall test of significance to the ensemble of
results obtained.
Fig. 5a–c From plant phenology to herbivore dynamics in Norway. Across large spatial scales, many plant species bloom earlier
following warm winters, which are characterised by a positive
NAO. a Annual dates of first flowering by Tussilago farfara vs
the NAO index, 1968–1977 (from Post and Stenseth 1999). As
yearlings, female red deer (Cervus elaphus) born following warm
NAO winters capitalise on early plant phenology during their first
spring to gain condition; consequently, they are more likely to
conceive than those born following cold winters. b Proportion of
female red deer in cohorts 1968–1977 that conceived as yearlings
vs the first flowering date of T. farfara in their year of birth (from
Post and Stenseth 1999). After these females produce their first
calves, the abundance of red deer in this population increases.
c Abundance of red deer in the current year vs the NAO index of
the winter 2 years before (from Forchhammer et al. 1998a; Post et
al. 1999a).
9
What does the NAO really explain?
In several of the examples given above, the relationship
between the NAO and an ecological descriptor is presented together with an underlying mechanism. However, besides these examples, there are still a number of
NAO-ecology relationships exhibiting strong statistical
significance but for which a causal mechanism has not
been clearly identified or proposed. Surprisingly, some
ecological groups for which physical forcing is generally
thought to be a major influence belong to this category.
This is, for example, the case for most studies on phytoplankton. The long-term (1985–1996) changes in phytoplankton biomass (measured as chlorophyll a) at a station in the mouth of the Gullmar Fjord in the eastern
Skagerrak reveal that phytoplankton biomass, primary
production and counts of three species of the toxic alga
genus Dinophysis are significantly correlated with the
NAO (Lindahl et al. 1998; Belgrano et al. 1999). Similarly, the changes in phytoplankton levels in the North
Sea described by Reid et al. (1998a, 1998b) show a weak
(but significant) correlation with the NAO. Furthermore,
both the Chrysochromulina bloom and the North Sea
seal epidemic in 1988 coincided with the change in regime reported by Reid et al. (in press) and earlier in this
study. These observations suggest that the occurrence,
formation and duration of toxic and non-toxic algal
blooms may be related to climatic variability at a regional scale, whereas the cause for the climate-phytoplankton
link remains unclear.
For terrestrial plants, the mechanisms are not always
explicit either. For example, the quality of wheat in the
UK has recently been related to the NAO index for the
months January–February by Kettlewell et al. (1999),
but no causal relationship has yet been clearly identified.
In Sweden, the changes in the faunal composition of
benthic foraminifers reported by Nordberg et al. (2000)
indicate a statistical relationship with the NAO but again
evidence of a mechanism is lacking.
While climate-ecology correlations are an important
first step towards explanation, many such relations have
broken in the past (as noted by, e.g. Myers 1998). Unless
a mechanistically based explanation is provided, the veracity of any statistical NAO-ecology relationship will
thus remain uncertain. However, finding the mechanisms
by which the NAO may influence ecological processes is
often the most difficult task.
The difficulty in identifying the causes of observed
relationships is particularly obvious in the case of the
NAO-Calanus relationship in the north-east Atlantic
(Fig. 2), although this strong relationship was one of the
first to be identified and has been intensively investigated. Four types of mechanism have been proposed to explain the strong correlation observed: changes in food
availability, alteration of the competition balance between C. finmarchicus and C. helgolandicus, variations
in the transport of individuals from the Faeroe-Shetland
Channel into the North Sea and reduction in the volume
of NSDW where the overwintering population resides
(Frometin and Planque 1996). Choosing between hypotheses like these is indeed not a trivial exercise.
Recommendations for how to study the ecological
effects of the NAO
Kröncke et al. (1998) and Heyen et al. (1998), following
the work of von Storch et al. (1993), have adopted a statistical downscaling approach to identify the plausible
mechanisms linking climate to changes in benthic communities. This approach starts from an exploratory analysis in which the statistical skill of a number of possible
combinations of predictors (environmental variables)
and predictands (biological variables) is inspected. The
retained combinations are cross-validated with independent new data and an investigation follows as to whether
a plausible mechanistic relationship can be proposed.
Such an approach is a step towards a better identification
of “true” NAO-ecology relationships. However, large exploratory analyses always reveal many statistically significant relationships and ecological processes are generally complex. Thus, among the relationships tested with
this method, a sizeable fraction of spurious ones will
likely not be detected as such.
The alternative “strategic cyclical scaling” strategy,
outlined in Root and Schneider (1995), which consists of
a “continuous cycling between strategically designed
large- and small-scale studies” is probably more powerful, as it clearly embeds small-scale process-oriented
studies in larger-scale investigations of a more statistical
nature.
In this review, we have underlined the difference between a statistically significant result and a result that is
biologically interpretable. This gap may be bridged
through the formulation of dynamic models used by, e.g.
Forchhammer et al. (1998b).
Conclusions and perspectives
We have shown that ecological components of the North
Atlantic and surrounding regions display a response at
species, population and community levels to climatic
variability. This review shows clearly that effects of the
NAO ripple through trophic levels from primary production to herbivores to predators, influencing growth, life
history traits and population dynamics along the way.
Documentation of the effects of the NAO on biological
processes gathered in this review should offer new insights relating to our understanding of the influence of
climate variability on both marine and terrestrial ecosystems.
As seen from the many examples presented in this review, the possible pathways by which the NAO may affect ecological processes show great variety. Summarising this variety emerging from a number of studies into a
restricted number of categories may prove fruitful. Here,
we suggest that the ecological effects of the NAO report-
10
Table 1 Examples of North Atlantic Oscillation (NAO)-ecology
relationships categorised by type of effect. Asterisks indicate studies invoking the NAO in their mechanisms. Although we have
tried to include as many papers of this category as possible, the list
should not be regarded as complete. Other cited works describe
mechanisms which we suggest to be influenced by the NAO
Ecological
descriptor
Type of effect
Parameter related
to the NAO
Suggested mechanism
Reference
UK and
US birds
Direct
Timing of egg laying
Alteration of physiological rates
(temperature effect)
UK
amphibians
Direct
Timing of spawning
Alteration of physiological rates
(temperature effect)
Terrestrial
plants
Direct
Timing of blooming/length of
production season
Alteration of physiological rates
(temperature, precipitation)
African
terrestrial
plants
Zooplankton
(Daphnia),
central Europe
Barents Sea
cod and
haddock
Sea trout fry,
Lake District,
UK
Barents Sea
cod and
haddock
Direct
Vegetation productivity
Alteration of physiological rates
(precipitation)
Crick et al. (1997); *
Forchhammer et al. (1998a);
McCleery and Perrins (1998);
Crick and Sparks (1999);
*Forchhammer and Post (2000);
Sæther et al. (2000);
*Wuethrich (2000)
Beebee (1995);
*Forchhammer et al. (1998a);
*Forchhammer and Post (2000)
Myneni et al. (1997);
Menzel and Fabian (1999);
*Post and Stenseth (1999)
*G. Oba et al. (2001)
Direct
Abundance
Alteration of physiological rates
(temperature)
Direct
Growth rate in early stages
Alteration of physiological rates
in larval and juvenile stages
Direct
Date of fry emergence
Unknown but linked to temperature *Elliott et al. (2000)
Direct/indirect
Recruitment levels
Direct/indirect
Quality
Regulates inflow of Atlantic water
to the Barents Sea, influencing
temperature and food availability
for the larval and juvenile stages
Delayed effect through rainfall
during August (?)
Unknown but linked to climate
and temperature. Possibly
modification of the timing of
spawning, and alteration of the
bioenergetic balance between
metabolic requirements and food
availability
Effect of winter temperature on
a predatory polychaete followed
by changes in predation rates on
two prey polychaete species
Modification of the competition
balance through alteration of
phytoplankton production and
change in sea surface temperature
Alteration of the circulation and
transport of individuals to the
North Sea
UK wheat
North Sea cod Direct/indirect
and plaice
Recruitment levels
Marine
polychaetes
Direct?/indirect Abundance
North Sea
zooplankton:
Calanus
species
North Sea
zooplankton:
Calanus
finmarchicus
European
flycatchers
(birds)
UK tits
(birds)
Indirect
Abundance
Indirect
Abundance
Indirect
Abundance
Indirect
Abundance
UK birds
Indirect
Spatial distribution
*Straile and Geller (1998);
*Straile (2000);
Straile and Adrian (2000)
Loeng et al. (1995);
Ottersen and Loeng (2000)
Ottersen et al. (1994);
Ottersen and Sundby (1995);
Ottersen (1996)
*Kettlewell et al. (1999)
Svendsen et al. (1995);
*Dippner (1998a, 1998b);
Planque and Frédou (1999);
C.J. Fox, B. Planque,
C.D. Darby, unpublished data
Beukema et al. (2000)
*Fromentin and Planque (1996)
Backhaus et al. (1994);
*Planque and Taylor (1998);
Stephens et al. (1998);
Heath et al. (1999)
*Sætre et al. (1999)
Modification of the competition
balance between pied and collared
flycatchers
Effect of early spring temperature Slagsvold (1975)
on population density through
juvenile survival rate, possibly
related to migration and/or
territorial behaviour
Migration northward in response to Thomas and Lennon (1999)
migration of prey (butterflies) in
response to temperature increase
11
Table 1 continued
Ecological
descriptor
Type of effect
Parameter related
to the NAO
Suggested mechanism
Reference
Netherlands
birds
Indirect
Timing of egg laying
Visser et al. (1998)
Norwegian
red deer
Indirect
Growth, breeding, density,
and sex ratios
Soay sheep
(Scotland)
Macrofaunal
community
Indirect
Abundance
Indirect
Abundance
European
sardine
and herring
Indirect
Abundance
Salmon
(rivers,
coastal waters,
open ocean)
Canadian
lynx
Moose and
white-tailed
deer
Wolf
predation
and moose
dynamics
Southern
Norway
dipper
(Cinclus
cinclus)
birds
Phytoplankton
(fjord, lake,
open ocean)
Indirect/
integrated
Salmon environment
Indirect/
integrated
Indirect/
integrated
Population phenology
Phenotypic selection on earlylaying birds in response to earlier
timing of food availability
Combination of alteration of
physiological rates, changes in the
timing and availability of food,
delayed effects through
density-dependent mechanisms,
in utero growth, fecundity
Winter survival combined with
density-dependent processes
Effect on surface primary
production transferred to the
bottom macrofaunal community
(Tunberg) or unspecified effect of
temperature (Kröncke)
Changes in temperature and wind
patterns causing regime shifts.
Changes in the pattern of transport
of herring in the North Sea
Various effects on rivers, coastal
waters and thermal habitat in
oceanic waters (again, little is
known about the mechanisms)
Uncertain; possibly alteration of
trophic interactions
Effect on winter survival and
density-dependent processes
Population dynamics
*Post et al. (1997, 1999a, 1999b,
1999c);
*Forchhammer et al. (1998b);
*Loison et al. (1999);
*Post and Stenseth (1999);
*Mysterud et al. (2000, in press)
*Milner et al. (1999);
*Post and Stenseth (1999)
*Kröncke et al. (1998);
*Tunberg and Nelson (1998)
*Alheit and Hagen (1997);
*Corten (1999)
Friedland et al. (*1993, 1998);
*Dickson and Turrell (1999);
*Reid and Planque (1999)
*Stenseth et al. (1999)
*Post and Stenseth (1998)
Indirect/
cascading
Winter pack size
Increased pack size and deeper
snow lead to higher kill rates and
declines in moose density
*Post et al. (1999c)
Indirect/
integrated
Population dynamics
Population dynamics and carrying
capacity respond to temperature
Sæther et al. (2000)
Indirect/
integrated
Abundance and production
Benthic
Indirect/
foraminifera, integrated
Gullmar Fjord,
Sweden
North Sea
Integrated
zooplankton:
Calanus
finmarchicus
Unknown (in Reid et al.,
the environmental factors which
might be responsible are given but
no clear mechanism is proposed);
mechanism(s) under study
Changes in faunal composition Effects of changes in oxygen
concentrations; mechanism(s)
not clear
*Reid et al. (1998a, 1998b);
*Belgrano et al. (1999);
*Weyhenmeyer et al. (1999)
Abundance
*Heath et al. (1999)
Reduction in the volume of
Norwegian Sea Deep Water where
C. finmarchicus overwinters
ed above can be classified according to three major
types: direct, indirect and integrated. (1) The direct effects of the NAO are mechanisms that involve a direct
ecological response to one of the environmental parameters synchronised with the NAO. The effect of the NAO
on metabolic rates via temperature is an example of this
type. (2) The indirect effects of the NAO are non-trivial
*Nordberg et al. (2000)
mechanisms that either involve several physical or biological intermediary steps between the NAO and the ecological trait and/or have no direct impact on the biology
of the population. (3) The integrated effects of the NAO
involve simple ecological responses that can occur during and after the year of an NAO extreme. This is the
case when a population has to be repeatedly affected by
12
a particular environmental situation before the ecological
change can be perceived (biological inertia) or when the
environmental parameter affecting the population is itself modulated over a number of years (physical inertia,
e.g. reduction in NSDW volume; Heath et al. 1999).
A series of examples of these effects, most of which
have been presented in this review, is summarised in Table 1 together with an indication of the type of effect involved in the NAO-ecology relationship. We distinguish
between mechanisms suggested by earlier authors to be
related to the NAO and earlier described mechanisms
which we propose to be influenced by the NAO.
Over the period of the instrumental record, the NAO
has exhibited considerable long-term variability (Hurrell
and van Loon 1997; see Fig. 1). Since the mid 1960s, an
increasing trend has been displayed, amplifying to the
most persistent and extreme positive phase ever observed in the late 1980s/early 1990s (Dickson et al.
1999). Furthermore, there are a number of indications
that the NAO is a much better proxy for North Atlantic
climate now than it has been in the past. This is of particular interest, since numerous models predict that the current positive phase of the NAO will persist at least for
the first decades of the 21st century (Paeth et al. 1999).
If this is the case, knowledge about the impact of the
NAO on ecology will be even more important in the near
future. However, investigations of large-scale ecological
phenomena and their underlying processes require longterm datasets and a cross-disciplinary perspective. This
is especially the case if we are to draw inferences about
possible climate change from studies of ongoing sources
of natural variability such as the NAO. All in all, we are
lead to conclude that ecologists as part of their investigations should include the possible effects of large-scale
climate patterns like the NAO.
Acknowledgements This work was partially financed through
grants from The Norwegian Research Council (G.O. and N.C.S),
The University of Oslo (N.C.S), the U.S. National Science Foundation (E.P.) and the European Commissions BASIS program
(FAIR PL 95 817; G.O.). A.B. acknowledges the European Commission for the award of a Postdoctoral Research Fellowship,
within the framework of the Marine Science and Technology programme (MAST III – contract MAS3-CT96-5028). A consortium
comprising IOC, UNIDO, the European Commission and agencies
from Canada, Denmark, France, The Netherlands, the Republic of
Ireland, the United Kingdom, and the USA supports the CPR survey (P.C.R.). We thank M.C. Forchhammer and A. Mysterud for
valuable comments.
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