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Phenological trends and trophic mismatch across multiple levels of a North Sea pelagic food web


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Differential phenological responses to climate among species are predicted to disrupt trophic interactions, but datasets to evaluate this are scarce. We compared phenological trends for species from 4 levels of a North Sea food web over 24 yr when sea surface temperature (SST) increased significantly. We found little consistency in phenological trends between adjacent trophic levels, no significant relationships with SST, and no significant pairwise correlations between predator and prey phenologies, suggesting that trophic mismatching is occurring. Finer resolution data on timing of peak energy demand (mid-chick-rearing) for 5 seabird species at a major North Sea colony were compared to modelled daily changes in length of 0-group (young of the year) lesser sandeels Ammodytes marinus. The date at which sandeels reached a given threshold length became significantly later during the study. Although the phenology of all the species except shags also became later, these changes were insufficient to keep pace with sandeel length, and thus mean length (and energy value) of 0-group sandeels at mid-chick-rearing showed net declines. The magnitude of declines in energy value varied among the seabirds, being more marked in species showing no phenological response (shag, 4.80 kJ) and in later breeding species feeding on larger sandeels (kittiwake, 2.46 kJ) where, due to the relationship between sandeel length and energy value being non-linear, small reductions in length result in relatively large reductions in energy. However, despite the decline in energy value of 0-group sandeels during chick-rearing, there was no evidence of any adverse effect on breeding success for any of the seabird species. Trophic mismatch appears to be prevalent within the North Sea pelagic food web, suggesting that ecosystem functioning may be disrupted.
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Mar Ecol Prog Ser
Vol. 454: 119–133, 2012
doi: 10.3354/meps09520 Published May 21
Phenology (the timing of seasonally recurring bio-
logical events) plays a crucial role in linking organisms
to their biotic and abiotic environments (Forrest &
Miller-Rushing 2010). Recent climate warming has
significantly altered the phenology of a wide range of
taxa across ecosystems (Thackeray et al. 2010), but re-
sponses frequently vary among species, potentially
disrupting the synchronisation of key ecological inter-
actions (Visser & Both 2005). In particular, failure of a
predator to overlap the period of peak resource de-
© Inter-Research 2012 ·*Email:
Phenological trends and trophic mismatch across
multiple levels of a North Sea pelagic food web
Sarah Burthe1,*, Francis Daunt1, Adam Butler2, David A. Elston3,
Morten Frederiksen1, 4, David Johns5, Mark Newell1, Stephen J. Thackeray6,
Sarah Wanless1
1Centre for Ecology & Hydrology, Bush Estate, Penicuik, Midlothian EH26 0QB, UK
2Biomathematics and Statistics Scotland, The Kings Buildings, Edinburgh EH9 3JZ, UK
3Biomathematics and Statistics Scotland, Craigiebuckler, Aberdeen AB15 8QH, UK
4Dept. of Bioscience, Aarhus University, Frederiksborgvej 399, 4000 Roskilde, Denmark
5Sir Alister Hardy Foundation for Ocean Science, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK
6Centre for Ecology & Hydrology, Lancaster Environment Centre, Bailrigg, Lancaster LA1 4AP, UK
ABSTRACT: Differential phenological responses to climate among species are predicted to dis-
rupt trophic interactions, but datasets to evaluate this are scarce. We compared phenological
trends for species from 4 levels of a North Sea food web over 24 yr when sea surface temperature
(SST) increased significantly. We found little consistency in phenological trends between adjacent
trophic levels, no significant relationships with SST, and no significant pairwise correlations
between predator and prey phenologies, suggesting that trophic mismatching is occurring. Finer
resolution data on timing of peak energy demand (mid-chick-rearing) for 5 seabird species at a
major North Sea colony were compared to modelled daily changes in length of 0-group (young of
the year) lesser sandeels Ammodytes marinus. The date at which sandeels reached a given
threshold length became significantly later during the study. Although the phenology of all the
species except shags also became later, these changes were insufficient to keep pace with sandeel
length, and thus mean length (and energy value) of 0-group sandeels at mid-chick-rearing
showed net declines. The magnitude of declines in energy value varied among the seabirds, being
more marked in species showing no phenological response (shag, 4.80 kJ) and in later breeding
species feeding on larger sandeels (kittiwake, 2.46 kJ) where, due to the relationship between
sandeel length and energy value being non-linear, small reductions in length result in relatively
large reductions in energy. However, despite the decline in energy value of 0-group sandeels dur-
ing chick-rearing, there was no evidence of any adverse effect on breeding success for any of the
seabird species. Trophic mismatch appears to be prevalent within the North Sea pelagic food web,
suggesting that ecosystem functioning may be disrupted.
KEY WORDS: Timing of breeding · Climate change · Prey size · Ammodytes marinus · Winter
NAO · Long-term studies · Zooplankton · Phytoplankton
Resale or republication not permitted without written consent of the publisher
Contribution to the Theme Section ‘Seabirds and climate change’
Mar Ecol Prog Ser 454: 119–133, 2012
mand (typically breeding) with peak prey availability
may lead to ‘trophic mismatch,’ and such decoupling
may alter food web structure and eco systems (Cushing
1990, Edwards & Richardson 2004). A recent review
found that trophic mismatch was widespread, with
predator phenology shifting too little or too much in
response to that of prey (Visser & Both 2005).
Marine systems are vulnerable to trophic mismatch
because they exhibit highly seasonal pulses of pri-
mary productivity upon which the fitness of higher
trophic levels depends (Cushing 1990). Studies
across multiple trophic levels are rare, mainly be -
cause phenological data at the appropriate temporal
and spatial resolution are lacking. Most
studies have investigated single species
responses and are unable to explicitly test for
mismatch (Leggett & DeBlois 1994). Studies
have also compared phenology of a focal
consumer with climate data such as sea-
surface temperature (SST; e.g. Durant et al.
2003, Frederiksen et al. 2004a, Shultz et al.
2009) that may indicate variation in prey
availability, including phenology, or be used
as a cue by predators to predict key pheno-
logical events in their prey (Frederiksen et
al. 2004a, Moe et al. 2009). Several studies
have suggested that mismatch may be an im -
portant determinant of fitness in seabirds
(e.g. Durant et al. 2006, Hipfner 2008, Wata -
nuki et al. 2009).
Here we examine phenological changes
across 4 trophic levels of a pelagic food web
in the north-western North Sea from 1983
through 2006. This system has a ‘wasp-waist’
structure (Cury et al. 2000), with high species
richness at upper and lower trophic levels
but markedly lower richness at the mid-
trophic position linking secondary producers
(zooplankton) and top predators (mammals,
fish and birds). Lesser sandeel Ammodytes
marinus occupies this key mid-trophic posi-
tion (Daan et al. 1990). Over the study period
there have been significant hydro-biological
changes and increased sea temperatures in
this area (Edwards et al. 2002). A major
ecosystem regime shift occurred in the late
1980s (Beaugrand 2004), and there have
been profound changes in plankton commu-
nities (Edwards et al. 2002) and fish distribu-
tions (Perry et al. 2005). Previous studies in
this area have investigated phenological
changes in species from primary producers
to top predators and found contrasting pat-
terns suggestive of trophic mismatch (Edwards &
Richardson 2004, Wanless et al. 2009, Frederiksen et
al. 2011). However, none have ad opted an integrated
ap proach and compared multiple trophic levels
within the same area over the same time period. A
major aim of our study was to use a standardised
approach to quantify changes in the timing of key
events for species or taxonomic groups across all 4
trophic levels (Fig. 1a). Disparity in phenological
trends would be indicative of trophic mismatch in the
system. We also assessed whether phenology was
related to climate variables (SST and winter North
Atlantic Oscillation, wNAO) and if climate res pon ses
Fig. 1. Schematic illustration of the different stages of analysis under-
taken: (a) analyses of the 4 trophic levels to examine trends in phe-
nology; trends between phenology and climate, and relationships be-
tween phenologies of adjacent trophic levels; (b) detailed analyses of
the seabird and sandeel data to examine phenological trends and the
impact of mismatch on breeding success. SST: sea surface tempera-
ture; wNAO: winter North Atlantic Oscillation; T: month (day of year)
of central tendency
Burthe et al.: North Sea trophic mismatch
were similar in terms of their magnitude and direc-
tion across the different trophic levels.
To investigate in more detail how the relative tim-
ing of trophically linked events have changed over
time, we focussed on 5 seabird species and their
major sandeel prey (Furness & Tasker 2000, Daunt et
al. 2008). Although trophic mismatch theory is most
often applied to the timing of peak prey abundance,
prey size is a key component and is known to be
important for seabirds in our study area (Wanless et
al. 2005). We therefore compared modelled annual
length-at-date of 0-group sandeels (Frederiksen et
al. 2011; sandeel hatched in the current year) with
the timing of peak energy demand in each seabird
species, which we assumed corresponded to the mid-
chick-rearing period (Drent & Daan 1980) (Fig. 1b).
Under this modified version of the mismatch hypo -
thesis our prediction was that mid-chick-rearing
should coincide with sandeels having attained a
threshold size, since individuals are expected to bal-
ance increasing prey quality through the season with
the fitness advantages of breeding as early as possi-
ble (Daunt et al. 2007, Harris et al. 2007). We
assessed whether the timing of chick-rearing had
become decoupled from seasonal changes in sandeel
length, and estimated mean size of fish at mid-chick-
rearing to quantify the consequences of mismatch on
prey energy value. Finally, we used the mismatch
index to explore the fitness consequences of mis-
matching on seabird breeding success.
Monthly average SST data were obtained from
NOAA Pathfinder Version 5.0 (Kilpatrick et al. 2001)
for an area of the North Sea (55 to 58°N, 3°W to 0°E)
between 1983 and 2006. Since spring events were our
main interest for comparison across the trophic levels
we focussed SST analysis on February and March
values (hereafter winter/spring SST). June and July
(hereafter summer SST) values were also modelled
with seabird breeding phenology as this period over-
lapped with mid-chick-rearing. As large-scale sea-
sonal measures of climate have been found to be use-
ful predictors of ecological processes (Hallett et al.
2004) and as 4 of the 5 seabird species being consid-
ered may be distributed outside the western North
Sea during winter, we also considered wNAO indices
( in dices.html) for the
winter prior to spring phenology events.
Phenology data
Phenology data were available across all trophic
levels between 1983 and 2006, and analyses were
thus restricted to this period.
Phytoplankton (primary producers) and
zooplankton (primary consumers)
The continuous plankton recorder (CPR) survey
is an upper layer plankton monitoring programme
(Richardson et al. 2006). We analysed a subset of
plankton data that are important in the diet of
sand eels Ammodytes marinus. Phytoplankton and
copepod nauplii are the main prey of larval sand -
eels (Monteleone & Peterson 1986), while older
stages of calanoid copepods (particularly Temora
spp. and Calanus spp.) are important for postlarval
stages, <10 cm in length (Macer 1966). According -
ly, we focussed on spring-peaking copepod species
(sandeel hatch date occurred mainly in February to
March) and ana lysed data for C. helgolandicus, C.
finmarchicus, T. longicornis, Calanus spp. Stages
I to IV, and copepod nauplii. Calanus spp. nauplii
feed preferentially on diatoms (Soreide et al.
2008). As there was no evidence that particular
diatom species were important for copepods, we
analysed the total summed monthly abundances
of the 10 most abundant diatoms in spring (indi-
vidual species data are presented in Table S1 of
the supplement at www.
m454 p119_ supp. pdf) and a colour in dex of phyto-
plankton. Data were obtained from an area of the
North Sea (55 to 58° N, 3° W to 0° E; Johns 2009)
that provided a balance between sampling reso lu -
tion and proximity to the Isle of May, Scotland
(56° 11’ N, 2° 33’ W), the focal point of sea bird
For plankton, the phenology measure was the
month of central tendency, T, (see Edwards & Rich -
ardson 2004) converted to day of year for compari-
son with other taxa. The average monthly abun-
dances over the 24 yr period for each species were
used to determine whether the seasonal pattern was
unimodal or bimodal (spring and autumn). For uni-
modal taxa, Twas calculated using data from the
entire year, whereas, for bimodal taxa, it was calcu-
lated using data from the first 6 mo of the year (see
Ed wards & Richardson 2004). Due to missing
monthly values for all species of plankton in 1995,
this year was omitted from plankton phenology
Mar Ecol Prog Ser 454: 119–133, 2012
Sandeels (secondary consumers)
Estimates of sandeel phenology (hatch dates) were
obtained from a statistical model implemented using
Markov Chain Monte Carlo procedures that com-
bined 2 time series of sandeel size at date data, i.e.
from larval fish captured during CPR surveys and 0-
group fish obtained from foraging puffins (see Fred-
eriksen et al. 2011 for full details).
Seabird predators
Analysis focussed on 5 species of seabirds for
which 0-group sandeels are an important dietary
component for adults and/or chicks on the Isle of
May (Daunt et al. 2008): common guillemot Uria
aalge (hereafter guillemot), razorbill Alca torda,
European shag Phalacrocorax aristotelis (hereafter
shag), black-legged kittiwake Rissa tridactyla (here-
after kittiwake) and Atlantic puffin Fratercula arctica
(hereafter puffin). Median egg dates were recorded
in guillemots and razorbills from daily checks of
monitoring plots (mean of ca. 800 and ca. 100 breed-
ing sites, respectively). For shags, annual median
ringing dates of chicks were analysed (mean ca. 800
chicks ringed mid-way through the chick-rearing
period at a mean age of 20 to 25 d) since median lay-
ing dates (estimated from weekly checks of ca. 100
pairs) were only available for a subset of years and
were strongly correlated with median egg date (r =
0.94, df = 20, p < 0.001). Kittiwake first egg dates
were analysed (from daily checks of the whole colony
of >3000 pairs) as median egg dates were only
recorded in a subset of years (from 5 d checks of ca.
200 pairs; correlation between first and median:
r = 0.90, df = 8, p < 0.001). First egg dates were also
analysed for puffins, back-calculated from daily
checks of the entire colony for adults bringing fish
back to chicks (>10 000 pairs; see Wanless et al. 2009
for details) since median egg dates (based on back-
calculation from wing and bill measurements of
chicks from a mean of ca. 30 individuals; see Harris &
Wanless 2011 for details) were only available for a
subset of years (correlation between first and
median: r = 0.61, df = 13, p = 0.015). Even though first
egg dates are likely to be subject to a higher level of
stochastic variation than median egg dates (Wanless
et al. 2009), they were assumed to be reliable indica-
tors of the timing of breeding for kittiwakes and
puffins because of the correlation with median egg
dates in the subset of years where both were
Phenological regressions
Standard linear regressions with year were used to
investigate temporal trends in SST, wNAO and phe-
nology of trophic levels. In order to avoid false detec-
tion of significant correlations due to multiple testing,
we applied the Benjamini & Hochberg (1995) correc-
tion factor to this set of models. In all cases we report
the uncorrected p-values. Phenology data for sandeel
hatch date showed evidence of a break-point (Fred-
eriksen et al. 2011), and were therefore analysed us-
ing a piecewise regression model employing the seg-
mented package in R (Muggeo 2008). In order to
assess whether the phenologies of consumers and
their prey covaried over time, we examined whether
there were pairwise correlations between phenolo-
gies of taxa across successive trophic levels. We in-
vestigated whether phenology was correlated with
climate by regressing the phenology of each species
against SST or wNAO. We analysed trends using sim-
ple linear regression, without taking temporal auto-
correlation into account, and thus assume that con-
secutive years are independent. Autocorrelation plots
of model residuals were examined and, in general,
showed no apparent evidence of autocorrelation,
suggesting that the assumption of independence was
reasonable. There was only 1 case (linear regression
of kittiwake first egg phenology and wNAO) in which
the regression coefficient was significant and the
model residuals showed evidence of autocorrelation.
Trophic mismatch in seabirds and sandeels
To evaluate phenological mismatch in greater
detail we focussed on interactions between seabirds
and 0-group sandeels, since, not only was the tempo-
ral resolution of these data markedly better than for
lower trophic levels, but information on other aspects
of performance such as sandeel growth rates and
seabird breeding success was also available. We
focussed on the peak period of energy demand for
the seabirds, i.e. the mid-point of the chick-rearing
period (Drent & Daan 1980). For shags this was esti-
mated directly from median chick ringing date as this
occurs midway through the chick-rearing period. For
guillemots and razorbills we used the species- and
year-specific median laying date plus the average
incubation period plus the average chick-rearing
period/2, while for kittiwakes and puffins we used
first egg date plus average difference between first
and median egg dates plus average incubation
period plus the average chick-rearing period/2. Val-
Burthe et al.: North Sea trophic mismatch
ues for incubation and fledging periods were ob -
tained from Cramp & Simmons (1978, 1983). The
average difference between first and median egg
dates was 11 d for kittiwake (range: 6 to 18 d, n = 10)
and 12 d for puffin (range: 6 to 17 d, n = 15).
The sandeel model (Frederiksen et al. 2011) esti-
mated mean hatch dates and growth rates, from
which daily size of juvenile sandeels was then esti-
mated. We compared relationships between the tim-
ing of mid-chick-rearing in seabirds and 2 phenolog-
ical metrics for sandeels: hatch dates and the date
each year that 0-group sandeels reached a predicted
mean threshold length of 55 mm. This was under-
taken because many phenological studies investi-
gate the timing of appearance of prey (hatch dates),
but we also wanted to test whether phenology of
sandeel size and hence prey quality was more rele-
vant to seabird predators. Other threshold sizes were
also analysed (Fig. S1 in the supplement at www.
int-res. com/articles/suppl/m454p119_supp. pdf), and
model fit was found to increase with sandeel size,
with 55 mm being the largest threshold size that
sandeels attained in all years of the study. Thus, this
was a useful measure to compare with timing of mid-
chick-rearing for each seabird species. Linear
regression with year was used to assess whether the
date sandeels reached 55 mm showed evidence of a
temporal trend.
In order to evaluate whether the timing of seabird
mid-chick-rearing had become decoupled from the
timing of availability of quality sandeel prey over the
study period, a ‘mismatch index’ was calculated as
the difference (in days) between the date of the mid-
point of chick-rearing for each seabird species and
the date that mean sandeel size was predicted to
reach the threshold of 55 mm. We emphasise that as
the mismatch index is based on a threshold sandeel
size, a mismatch index of 0 does not indicate perfect
matching of predator and prey timing. Instead posi-
tive values of the index indicate that the seabirds’
peak energy demand occurred after sandeels
reached 55 mm, while negative values indicated that
peak demand preceded this threshold being at tained.
Thus, more positive values potentially indicated bet-
ter matching with higher quality prey (larger fish)
and more negative values indicated peak demand co-
inciding with poorer quality prey. We assessed tem-
poral changes in this mismatch index for each seabird
species using linear regressions with year. Finally, we
estimated mean sandeel size at mid-chick-rearing to
quantify the effects of mismatch on prey energy value
using the equation relating sandeel length to energy
value from Hislop et al. (1991). Due to the non-linear
nature of this relationship, declines in size of large
fish are more energetically costly than similar
declines in smaller fish. Linear regression with year
assessed whether there had been any systematic
change in sandeel size at this time.
Generalised linear modelling was used to evaluate
whether changes in seabird breeding success were as-
sociated with sandeel phenology and mismatch para-
meters, selecting models by Akaike’s information cri-
terion corrected for small sample sizes (AICc; Hurvich
& Tsai 1989, Burnham & Anderson 2002). Breeding
success was defined to be the ratio of the total number
of chicks fledged to the total number of chicks that
could potentially have fledged (a proportion). The
total number of chicks that could potentially have
fledged is equal to the maximum brood size multiplied
by the total number of nests at which eggs were laid.
Maximum brood size is invariably 1 for guillemots, ra-
zorbills and puffins, and typically 3 for kittiwake and 4
for shag (Cramp & Simmons 1978, 1983). Details of
sample sizes and field methodology for monitoring
breeding success are given in Harris et al. (2005). In
addition to the sandeel phenology and mismatch para -
meters (sandeel hatch date, sandeel growth rate,
length of sandeels at the mid-point of chick-rearing
and mismatch index) we also included in model selec-
tion the following extrinsic factors that have previously
been shown to correlate with breeding success for
these seabird species on the Isle of May (Frederiksen
et al. 2004b, 2006): lagged sandeel biomass index (an
annual index modelled from the probability of sand eel
larvae occurring in CPR samples and summed mass of
larvae in a sample; see Frederiksen et al. 2006 for de-
tails); lagged SST (previous year) and sandeel fishery
presence (kittiwake only; Frederiksen et al. 2008).
As the sandeel variables (apart from sandeel bio-
mass index) arise from the same statistical model
(Frederiksen et al. 2011; see Table S3 in the supple-
ment at p119_
supp.pdf) we inclu ded at most one of these variables
in each model. We used summed Akaike weights to
calculate the relative strength of support for each of
the potential predictors. Note that sandeel phenology
and mismatch parameters each appeared in 8 of the
40 models within the candidate set (a prior weight
of 0.2), whereas the variables relating to extrinsic fac-
tors each appeared in 20 of the 40 models (a prior
weight of 0.5) —this difference must be taken into ac-
count when drawing comparisons between the 2
groups of variables.
Regression models were applied to logit-trans-
formed data on breeding success for guillemot, razor-
bill and puffin, and to log-transformed data for
Mar Ecol Prog Ser 454: 119–133, 2012
kittiwake and shag, as well as being applied to
untransformed data for all species. The same models
(i.e. the same sets of explanatory variables) were
selected by AICc for both transformed and untrans-
formed data; we present the results for the untrans-
formed data solely in order to allow direct compari-
son with the results of Frederiksen et al. (2006). We
considered the inclusion of quadratic, as well as lin-
ear, relationships and sandeel parameters lagged by
1 yr, but found no support for inclusion of these
terms. Spurious relationships between an explana-
tory variable and the response variable can arise if
both are correlated with a third variable, particularly
time (Grosbois et al. 2008). We therefore included
year as an explanatory variable in order to assess
whether the same best model was selected once year
was included, and whether the addition of year
improved model fit.
Winter/spring SST increased by an average (±SE)
of 0.056 ± 0.014°C yr−1; p < 0.001, an in crease of
1.34°C over the study period. Summer SST also in -
creased significantly (overall increase: 1.42°C; 0.059
± 0.016°C yr−1; p = 0.002). In contrast, there was no
significant trend in the wNAO (estimate: −0.097 ±
0.060; p = 0.118; Fig. 2).
Phenological trends
For primary producers, neither the timing of the
seasonal peak of overall summed phytoplankton
abundance, nor that of the colour index showed a sta-
tistically significant trend (Fig. 3). Similarly, phenol-
ogy of primary consumers appeared to be largely
unchanged and only 1 species, Temora longicornis,
showed a significant advancement in timing. Sand -
eel Ammodytes marinus hatch date showed, within
the piecewise regression model, a highly significant
break-point in 1995 (95% CI from 1991 to 1998,
p = 0.001; model R2= 0.452), with hatching initially
becoming later and then becoming earlier (Fig. 3).
With the exception of shags, whose timing varied
greatly from year to year, seabird breeding tended to
become later, with significant trends for guillemot
and kittiwake (Fig. 3). All significant trends re -
mained significant after the Benjamini and Hochberg
correction factor was applied to this set of models.
Winter/spring SST
Summer SST
1990 2000
wNAO index Mean SST (ºC)
Trend (days per decade)
Phytoplankton colour index
Summed phytoplankton
Calanus stages I-IV
Temora longicornis
Calanus finmarchicus
Calanus helgolandicus
Copepod nauplii
Sandeel hatch date (1983 to 1995)
Sandeel hatch date (1995 to 2006)
Guillemot median egg
Razorbill median egg
Shag median ringing
Kittiwake first egg
Puffin first egg
Fig. 3. Phenology trends (negative values below the line in-
dicate timing becoming earlier, and positive values above
the line indicate timing becoming later; n = 23 for plankton
species and n = 24 for sandeel and seabirds) for species/
groups from the 4 trophic levels with standard errors
(trophic levels are shaded differently: palest grey: primary
producers; darkest grey: top predators) in a North Sea
pelagic food web between 1983 and 2006. Significant
trends after correction (p < 0.05)
Fig. 2. Mean winter/spring and summer sea-surface temper-
ature (SST) values, and the winter North Atlantic Oscillation
(wNAO) index score over the study period. Fitted lines show
significant regressions
Burthe et al.: North Sea trophic mismatch
Phenological regressions with climate
Overall there was little evidence that trends in phe-
nology were associated with either of the climate
variables. Significant relationships between phenol-
ogy and winter/spring SST (see Table 1) for Temora
longicornis and Calanus spp. Stages I to IV were
apparent, but did not remain significant after apply-
ing the Benjamini and Hochberg correction to this set
of models. None of the regressions were significant
between seabird egg-laying phenology and winter/
spring SST (Table 1) or summer SST (guillemot:
t= 0.50, p = 0.62; razorbill: t= −1.22, p = 0.24; shag:
t= −0.69, p = 0.50; kittiwake: t= 0.911, p = 0.37;
puffin: t= 0.40, p = 0.70). Phytoplankton colour index,
but not summed abundance, was positively related to
wNAO, while timing of guillemots, razorbills and
kittiwakes showed a negative relationship. Only the
regression with kittiwake pheno logy remained
significant once the correction factor had been
applied to this set of models. How-
ever, this model also showed some
evidence of autocorrelation when
model resi duals were examined and
hence should be interpreted with
Comparisons of phenological
change among trophic levels
There was no evidence that pre -
dator and prey phenologies were
related, with no significant pairwise
regressions between any of the tro -
phic comparisons (the significant re -
lationship between sandeel hatch
and timing of peak abundance
of Cala nus helgo landicus was no
lon ger significant after correction
(Table 2 and Table S2 in the supple-
ment at articles/
suppl/ m454 p119_supp. pdf).
Phenology measure n Day of year Spring SST wNAO
Mean SD Slope SE p R2Slope SE p R2
estimate (%) estimate (%)
Phytoplankton colour T23 103.00 11.09 −1.89 3.82 0.63 1.16 2.54 1.04 0.02 22.20
Summed phytoplankton T23 98.35 11.24 −1.32 3.88 0.74 0.55 −0.86 1.18 0.47 2.50
Calanus spp. Stages I to IV T23 115.65 15.73 −10.40 4.95 0.05 17.35 1.18 1.65 0.48 2.39
Temora longicornis T 23 120.35 15.72 −12.64 4.70 0.01 25.66 0.29 1.67 0.86 0.14
C. finmarchicus T 23 96.09 14.65 −3.66 5.01 0.47 2.48 −0.37 1.55 0.82 0.26
C. helgolandicus T 23 66.70 26.82 12.64 8.88 0.17 8.81 3.97 2.71 0.16 9.26
Copepod nauplii T23 123.87 13.00 0.80 4.50 0.86 0.15 −0.28 1.38 0.84 0.20
Sandeel hatch date 24 71.44 9.03 0.52 3.12 0.87 0.13 0.93 0.90 0.31 4.65
Date sandeels reach 55 mm 24 162.17 16.45 7.62 5.45 0.18 8.18 −1.88 1.62 0.26 5.79
Guillemot median egg 24 128.13 3.79 0.71 1.30 0.59 1.33 −0.93 0.33 0.01 26.28
Razorbill median egg 24 130.17 3.69 −0.76 1.26 0.55 1.63 −0.76 0.34 0.03 18.93
Shag median ringing 22 132.55 19.82 −7.14 5.96 0.24 6.13 0.71 1.80 0.70 0.70
Kittiwake first egg 24 131.50 8.46 1.37 2.91 0.64 0.99 −2.35 0.70 0.00 34.14
Puffin first egg 24 99.88 5.10 1.59 1.73 0.37 3.68 −0.70 0.50 0.17 8.41
Table 1. Linear regressions of phenology against mean winter/spring sea-surface temperature (SST) and winter North Atlantic
Oscillation (wNAO), together with uncorrected p-values. Significant regressions (at the 5% level, after applying the Benjamini
and Hochberg correction factor) are highlighted in bold. T: central tendency for monthly plankton data
Response Explanatory Slope SE t p
Calanus finmarchicus T Phytoplankton colour T −0.476 0.269 −1.768 0.092
C. helgolandicus T Phytoplankton colour T −0.119 0.527 −0.227 0.823
Calanus stages T Phytoplankton colour T 0.277 0.304 0.914 0.371
Temora longicornis T Phytoplankton colour T 0.282 0.303 0.929 0.363
Copepod nauplii T Phytoplankton colour T 0.258 0.250 1.032 0.314
Sandeel hatch C. finmarchicus T 0.038 0.111 0.344 0.734
Sandeel hatch C. helgolandicus T 0.128 0.054 2.377 0.027
Sandeel hatch Calanus stages T 0.096 0.101 0.949 0.354
Sandeel hatch T. longicornis T −0.011 0.103 −0.110 0.913
Sandeel hatch Copepod nauplii T −0.175 0.119 −1.469 0.157
Sandeel hatch Phytoplankton colour T −0.056 0.146 −0.380 0.708
Guillemot median egg Sandeel hatch 0.034 0.089 0.376 0.711
Razorbill median egg Sandeel hatch 0.075 0.086 0.874 0.392
Shag median ring Sandeel hatch −0.332 0.414 −0.802 0.431
Kittiwake first egg Sandeel hatch 0.088 0.199 0.440 0.664
Puffin first egg Sandeel hatch 0.106 0.118 0.893 0.382
Table 2. Linear regressions of phenology of upper trophic level species/group against
that of the relevant lower trophic level, together with uncorrected p-values. Results for
summed total phytoplankton abundance were similar to the colour index (see Table S2
in the supplement at supp. pdf). Tis the
central tendency for monthly plankton data
Mar Ecol Prog Ser 454: 119–133, 2012
Trophic mismatch in seabirds and sandeels
The date at which 0-group sandeels reached a pre-
dicted mean threshold length of 55 mm became sig-
nificantly later, at an average rate of 13.1 d decade−1
over the study period (Fig. 4). The date of mid-chick-
rearing was significantly related to the estimated date
this threshold length was reached for 4 of the seabird
species (guillemot, razorbill, puffin and kittiwake;
Fig. 5), and relationships for guillemot, razorbill and
kittiwake remained significant even when year was
also included in the model. However, the regression
coefficient (slope) of mid-chick-rearing against the
date sandeel threshold length was reached was sub-
stantially less than unity for these species (Fig. 5). This
indicated that although mid-chick-rearing had be-
come later in these 4 species, the shift in timing of
sandeel size had been even faster. Razorbills showed
the slowest rate of change in timing of breeding, and
kittiwakes, the fastest. In contrast, shags showed no
temporal trend in breeding phenology or relationship
with sandeel size phenology (Fig. 5).
In addition to differing rates of phenological
change, there was also interspecific variation in the
1985 1990 1995 2000 2005
1 Jun 1 Jul 1 Aug
Slope = 13.1 days per decade
R2 = 31.6%
p = 0.004
Date sandeels reached 55 mm
1 Jun 1 Jul 1 Aug
1 Jun 1 Jul 1 Aug
Slope = 1.5 days per decade
R2 = 42.5%
p < 0.001
Slope = 1.2 days per decade
R2 = 30.5%
p = 0.005
p = 0.73
1 Jun 1 Jul 1 Aug 1 Jun 1 Jul 1 Aug
1 Jun 1 Jul 1 Aug 1 Jun 1 Jul 1 Aug 1 Jun 1 Jul 1 Aug
Slope = 3.3 days per decade
R2 = 42.3%
p < 0.001
Slope = 1.4 days per decade
R2 = 21.7%
p = 0.022
Date predicted mean sandeel sizes reached 55 mm threshold
Date of mid chick-rearing
Fig. 4. Regression between the date that mean sizes of
sandeel Ammodytes marinus are predicted to attain a
threshold of 55 mm and year. The line shows the significant
fitted regression. Relationship remained significant even
when the latest date sandeels reached 55 mm (in 2004,
dotted circle) was removed from the analysis
Fig. 5. Regressions between the
date of peak chick demand and the
date that predicted mean sizes of
sandeel Ammodytes marinus reach
a threshold of 55 mm. Lines show
significant fitted regressions, and
relationships remained significant
even when the latest date sandeels
reached 55 mm (in 2004, dotted cir-
cle) was removed from the analysis
Burthe et al.: North Sea trophic mismatch
absolute timing of breeding. Ranking of the timing of
breeding for 4 of the 5 seabird species was generally
constant across the study period, with puffins and
guillemots breeding earliest, followed by razorbills,
and with kittiwakes breeding last. In contrast, shag
mid-chick-rearing was highly variable, being the
earliest studied bird in 3 of the years and the latest in
9 of the years.
These disparities in absolute timing and rates of
change in seabird breeding schedules and sandeel
sizes were integrated in the mismatch index (Fig. 6).
Thus, in the 1980s, mid-chick-rearing for all the
species considered occurred well after 0-group
sandeels reached 55 mm (positive values of the mis-
match index), whereas, in recent years, mid-chick-
rearing coincided with (mismatch index around 0)
or oc curred before (negative values) the date at
which sand eels had attained this size in 4 of the 5
seabird species. Kittiwakes were the exception; they
bred latest and hence had generally higher mis-
match index values than the other species (Fig. 6).
As a result, the mean length of 0-group sandeels at
mid-chick-rearing has significantly decreased over
the study period in all seabird species (Fig. 7). The
total estimated decrease over 24 yr and rates of de -
cline (±SE) were as follows: for guillemots: 10.2 mm,
−0.44 (±0.16) mm yr−1; for razorbills: 12.4 mm, −0.54
0.16) mm yr−1; for shags: 21.7 mm, −0.94 (±0.28)
mm yr−1; for kittiwakes: 10.2 mm, −0.44 (±0.19) mm
yr−1; and for puffins: 10.7 mm, −0.47 (±0.15) mm
Chick rearing
before sandeels after sandeels
= 55 mm = 55 mm
Sandeel size
1985 1990 1995 2000 2005
Shag Kittiwake
1985 1990 1995 2000 2005
1985 1990 1995 2000 2005
1985 1990 1995 2000 2005 1985 1990 1995 2000 2005
Mismatch index (days)
Fig. 6. Temporal changes in mismatch index (difference in days between timing of seabird mid-chick-rearing and the mean
date that sandeels Ammodytes marinus were predicted to reach a threshold of 55 mm). As shown in upper left panel, a nega-
tive index means that mid-chick-rearing occurred before sandeels attained a threshold length of 55 mm; hence, sandeels
would have been 55 mm and smaller during chick-rearing. Positive index values indicate that mid-chick-rearing occurred af-
ter this threshold; hence, sandeels would have been 55 mm or larger during chick-rearing. Solid lines: significant fitted regres-
sions; dashed line (kittiwakes): non-significant. We emphasise that because the mismatch index is based on a threshold size of
sandeel, a value of 0 for the mismatch index does not indicate perfect matching between seabirds and sandeels; rather the
higher the mismatch index the larger the sandeels available
Mar Ecol Prog Ser 454: 119–133, 2012
yr−1. Shags, with the steepest rate of predicted
decline, showed the highest net reduction in en -
ergetic value of fish over the 24 yr study period
(4.80 kJ, a 70.4% decline from 1983). Despite kitti-
wakes having the lowest rate of decline in sand eel
size, this species showed the next highest overall
reduction in net energetic value of 2.46 kJ (42.2%
decline from 1983). As the latest breeding seabird,
mid-chick-rearing of kittiwakes occurred when
sandeels were predicted to be larger and, due to the
non-linear nature of the relationship between sand -
eel length and energetic content, declines in the
length of large fish are more ener getically costly
than equivalent declines in smaller fish. Net de -
clines in the energetic value of fish were 1.70 kJ
(46.7%) for guillemot, 2.21 kJ (52.4%) for razorbill
and 1.79 kJ (48.2%) for puffin.
Consequences of mismatch for seabird
breeding success
Despite the energetic implications associated with
the pronounced decline in 0-group sandeel length
at mid-chick-rearing, there was no evidence that
this or sandeel hatch date had a significant effect on
the breeding success of any of the 5 species of
seabirds considered once other significant variables
were in cluded in the models. The breeding success
of guillemot, razorbill and shag was, however, posi-
tively related to sandeel growth rates (slope esti-
mates ± SE: 0.849 ± 0.204, 0.341 ± 0.193, and 0.729 ±
0.333, respectively) such that in years with poorer
sandeel growth these species had poorer breeding
Breeding success for shags, kittiwakes and puffins
was poorer in years following a year with warmer
winter/spring SST (slope estimates ± SE: −0.101 ±
0.042, −0.126 ± 0.030, −0.108 ± 0.028, respectively)
and higher following years with a high sandeel bio-
mass index (slope estimates ± SE: 0.047 ± 0.020, 0.035
± 0.018, and 0.032 ± 0.013, respectively). All species
ex cept kittiwake showed evidence of a linear trend
(negative for all species except shag) in success over
time that was not accounted for by the other model
variables (Table 3). The inclusion of quadratic or
lagged sandeel terms did not lead to models with
lower AICc values.
R2 = 27.3%
p = 0.009
R2 = 35.2%
p = 0.002
1985 1990 1995 2000 2005
R2 = 35.7%
p = 0.003
1985 1990 1995 2000 2005
R2 = 20.6%
p = 0.026
1985 1990 1995 2000 2005
1985 1990 1995 2000 2005 1985 1990 1995 2000 2005
R2 = 30.5%
p = 0.005
Size of sandeels at mid-point of chick rearing (mm)
Fig. 7. Predicted size (mm) of
Ammo dytes marinus sandeel at date
of mid-chick-rearing for each sea -
bird species over the study period
Burthe et al.: North Sea trophic mismatch
Phenological changes across trophic levels
To our knowledge, this is the first direct comparison
of phenologies across multiple trophic levels of the
North Sea pelagic food web. We found contrasting
trends across the 4 trophic levels that were suggestive
of trophic mismatch, supporting the assertion from
other studies that this phenomenon is widespread
(Visser & Both 2005). However, in contrast to mis-
match theory for marine systems (Cushing 1990) and
empirical results from terrestrial studies (Visser &
Both 2005, Both et al. 2009), we found no evidence of
strong pairwise relationships between predator and
prey phenologies, except for timing of mid-chick-
rearing in some seabird species and threshold size of
0-group sandeels Ammodytes marinus, and hence no
evidence of matching in this system. This suggests
that phenologies of North Sea species may have been
mismatched since at least 1983, which is possible as
most of our study followed the abrupt increase in SST
and regime shift in the late 1980s (Beaugrand 2004).
Contrasting phenological responses can arise for
several reasons. For example, if organisms at differ-
ent trophic levels vary in their ability to respond to
climate warming or in the extent to which their phe-
nology is influenced by alternative drivers. The ab -
sence of significant relationships be tween any of the
phenology metrics considered and SST, apart from
suggestive relationships with Cala nus spp. stages
and Temora longicornis, suggests that differential re -
s ponses to climate warming may be unimportant, at
least in this part of the western North Sea. Alterna-
tively winter/ spring or summer SST may not be at the
appropriate temporal or spatial scale for elucidating
such responses. Indeed, there was evidence that
timing of breeding for 3 of the 4 sea birds that dis-
perse outside the North Sea in winter (kittiwakes,
guillemot and razorbills, but not puf fins) was related
to broader scale climate cues (wNAO), particularly in
the case of the kittiwake which ex hibits the widest
dispersal (Wernham et al. 2002, Bogdanova et al.
2011). High abundance and/or broad peaks of sea-
sonal prey can potentially mask phenological rela-
tionships (Durant et al. 2005), with phenological
matching likely to be particularly apparent when
prey abundance is reduced or only available for a
short duration of time. In the North Sea, dramatic
changes in abundance and spatial distributions of
phytoplankton and copepods (Beaugrand et al. 2009)
have been observed. However, patterns of change
are not consistent within trophic levels, with in -
creases apparent for some species (for example
C. helgolandicus), while others are decreasing (e.g.
C. finmarchicus) (Planque & Fromentin 1996). Thus it
is unclear to what extent changing abundance may
be masking phenological matching in our system.
Finally, there may potentially be lagged responses of
predators to prey phenology such that comparison of
phenologies in the same year does not elucidate rela-
tionships. For example, phenology of juvenile zoo-
plankton abundance is related to the reproductive
timing of parent generations (Ellertsen et al. 1987).
Predictor No. of models Guillemot Razorbill Shag Kittiwake Puffin
Sandeel size 8 / 40 0.001 0.125 0.083 0.135 0.125
Sandeel hatch date 8 / 40 0.025 0.090 0.099 0.071 0.171
Sandeel growth rate 8 / 40 0.966 0.364 0.319 0.176 0.097
Mismatch index 8 / 40 0.004 0.135 0.110 0.019 0.121
Sandeel biomass index lagged 20 / 40 0.169 0.237 0.560 0.872 0.679
SST lagged 20 / 40 0.177 0.116 0.477 0.985 0.979
Year (linear time trend) 20 / 40 0.956 0.924 0.507 0.585
Sandeel fishery presence 20 / 40 0.847
R2for model with lowest AICc (%) 71.80 50.85 49.9 65.38 71.30
n (yr) 2424212224
Table 3. Importance of variables associated with seabird breeding success, based upon summed Akaike weights (range from 0
to 1; high values indicate strong support), were calculated using the full candidate set of n = 40 models (see Table S4 in the
supplement at Note that parameters derived from the sandeel model
(hatch date, growth rate, size and mismatch index) were present in 8 of the 40 models within the candidate set, whereas the
remaining predictors were present in 20 models —the prior weights for these variables are therefore 0.2 and 0.5, respectively,
and this difference needs to be taken into account when drawing comparisons between the 2 groups of variables. Predictors
included in the model with the lowest value of the corrected Akaike’s information criterion (AICc) for each species are shown
in bold, and we report the overall R2values for these models. SST: sea-surface temperature
Mar Ecol Prog Ser 454: 119–133, 2012
It is also possible that sampling differences be -
tween the trophic levels could potentially result in
phenology measures that are too crude to identify
correlations. The plankton data were at a lower tem-
poral resolution and broader spatial scale than the
sandeel and seabird data, and central tendency esti-
mates of plankton phenology are known to have low
sensitivity if timing shifts are small (Ji et al. 2010).
Moreover, copepods may respond to timing of critical
abundance thresholds of diatoms, rather than to sea-
sonal peaks (Runge et al. 2005). In addition, we con-
sidered mean phenological values at a broad spatial
scale, whereas changes in prey distributions can lead
to localised spatial mismatch (Schweiger et al. 2008).
Ideally future analyses of phenological trends and
mismatch in this system should account for annual
variation in prey abundance by investigating overlap
between distributions of prey availability and preda-
tor peak energetic demands rather than treating
them as point estimates.
Trophic mismatch between seabirds and sandeels
A key finding of the present study was that, for most
of the Isle of May seabird populations considered, the
timing of seabird mid-chick-rearing tracked the timing
of 0-group sandeels attaining a threshold size, rather
than sandeel hatch dates per se. The rate at which
mid-chick-rearing was delayed varied among the spe-
cies, but in all cases was insufficient to keep pace with
the delayed date at which sandeels attained a thresh-
old size. The net result was that for all 5 seabird spe-
cies the size of 0-group sand eels around the mid-point
of chick-rearing, when energetic requirements are
likely to be greatest, has significantly declined.
The seabird species we considered differed to
some extent as to the importance of 0-group sand eels
in adult and chick diets, with the likely ranking in
decreasing order of reliance being kittiwake, puffin,
razorbill, guillemot and shag (Daunt et al. 2008). This
ranking reflects the species- specific differences
apparent in mismatching, with kittiwakes, which
show the greatest reliance on the 0-group, tracking
changes in size most closely, while shags, for which
the 0-group is a minor part of the diet, showed no
trend in their breeding phenology. However, the pre-
dicted net energetic re duction in 0-group sandeel
prey was higher for kittiwakes than for the other
seabird species that were also tracking changes in
sandeel size, despite kittiwakes showing the greatest
phenological shifts in re sponse to changing sandeel
timing. This is be cause variation in net energetic
costs of reductions in sandeel size also depends on
the absolute tim ing of breeding. As the consistently
latest bree d ing seabird on the Isle of May, kittiwake
mid-chick-rearing occurred when sandeels were
predic ted to be larger and, due to the non-linear
nature of the relationship between sandeel length
and energetic content, declines in the length of large
fish are more energetically costly than equivalent
declines in smaller fish.
Although the results presented here pertain to
seabirds from the Isle of May, the order and annual
timing of breeding for the species considered were
consistent and varied in parallel with another North
Sea colony 90 km distant (Wanless et al. 2009). This
suggests consistency, at least at the local scale, with
seabirds from these 2 colonies potentially foraging on
the same sandeel stock. However, qualitative data
from other UK seabird colonies suggests that breed-
ing phenology may vary considerably between loca-
tions (Wanless et al. 2009). Moreover, sandeel popu-
lations also exhibit significant regional variation in
growth rates, length-at-age and abundance (Boulcott
et al. 2006), and further work is needed to identify
whether interactions between seabirds and sandeel
phenology vary regionally.
Very few other studies have considered the role of
prey quality in trophic mismatch. However, Beau-
grand et al. (2003) found a mismatch between the
size of larval cod Gadus morhua relative to the size of
their calanoid copepod prey, resulting in poorer cod
survival. Similarly, in a terrestrial system, caribou
Rangifer tarandus births had become mismatched
from the onset of newly emergent nutrient-rich plant
growth, resulting in reduced offspring survival (Post
& Forchhammer 2008). There are several potential
reasons why Isle of May seabirds are failing to track
changes in the timing of 0-group sandeel size. Firstly,
the cues used by the birds to time their breeding may
not accurately predict 0-group sandeel phenology.
Secondly, there may be trade-offs between the bene-
fits of delaying breeding to maintain 0-group sandeel
size and the fitness benefits of early breeding (Daunt
et al. 2007, Harris et al. 2007). Thirdly, the birds may
be constrained in their ability to alter their phenology
due to having a photoperiodically controlled physio-
logical window of breeding timing (Dawson 2008).
Finally, adult birds may compensate for the lower
energy value of 0-group sandeels by increasing for-
aging effort and/or switching to alternative prey. It is
probable that some, possibly all, of these factors are
operating in our study system.
Despite the apparently serious implications in
terms of the reduced energy value of prey associated
Burthe et al.: North Sea trophic mismatch
with changes in 0-group sandeel length at the time of
chick-rearing, particularly for kittiwakes, there was
no evidence that this was related to poorer breeding
success. This contrasts with studies from a Norwe-
gian seabird colony where breeding success of
puffins was positively related to the size of herring
prey (Durant et al. 2003) and from a Japanese colony
where rhinoceros auklet Cerorhinca monocerata
breeding success was poorer in years when birds
were mismatched from the availability of their prey,
Japa nese anchovy Engraulis japonicus (Watanuki et
al. 2009). The reason for this disparity is currently
unclear, but may well be linked to differences in
the life-history traits of the species involved, hydro-
biological characteristics of the study systems — with
both the mismatch examples given above being from
a conveyor-type system where prey availability is
affected by the timing of currents and whether
other factors such as predation or severe weather
exert a major effect on breeding success.
It is also plausible that breeding success of some
Isle of May seabirds is more closely linked to the
scheduling and/or abundance of one or more alterna-
tive prey species. The main alternative prey species
for Isle of May seabirds are 1+-group sandeels, clu-
peids (predominantly sprats Sprattus sprattus) and
butterfish Pholis gunellus (Daunt et al. 2008). Time
series data on abundance or phenology for these spe-
cies are lacking; thus, it is impossible to repeat the
approach used to look for matching between seabird
breeding and 0-group sandeels. Previous findings
suggest that the timing of 1+-group sandeel abun-
dance is potentially important for kittiwakes, guille-
mots and shags (Frederiksen et al. 2004b). Our
analyses of breeding success included a range of
potentially important variables, and results indicated
that these differed among the species. Sandeel abun-
dance as indicated by a sandeel biomass index and
the sandeel growth rate, which may be linked with
behavioural changes and hence availability of sand -
eel to seabirds, emerged as being consistently im -
portant. However, we emphasise that investigating
breed ing phenology in relation to prey phenology
assumes that this is the single critical activity under
selection (Visser & Both 2005). In reality, the entire
life-cycle is under selection and responding to multi-
ple environmental drivers, such that breeding phe-
nology may be the outcome of trade-offs between
several selection pressures. Ideally, in future work,
multiple life-history traits should be investigated at
the individual level to understand whether predators
are adequately responding to changes in prey phe-
nology and the fitness costs of mismatch.
Quantifying the shift in the phenology of a prey
species has been suggested as an appropriate yard-
stick for interpreting whether a predator is shifting its
phenology adequately to match the change in its
environment often as a result of climate change
(Visser & Both 2005). Our study followed this ap -
proach to assess phenological changes across multi-
ple trophic levels of the pelagic food web in the west-
ern North Sea. At a broad spatial scale we found
contrasting phenological trends between trophic
levels that may indicate that the system is currently
experiencing trophic mismatching. By developing a
novel approach we also explored finer scale data on
the timing of peak energy for avian predators in rela-
tion to temporal changes in the energy value of an
important piscivorous prey. This analysis highlighted
significant changes over 24 yr in temporal matching
of the chick-rearing periods of 5 species of seabirds
and in the size of 0-group sandeels such that prey
length, and hence energy value of individual items,
have declined significantly. To date, there is no evi-
dence that these changes are impacting on the
breeding success of any of the seabird species con-
sidered, but further changes, particularly if alterna-
tive prey are also affected adversely, could well have
population level consequences for the North Sea
seabird community.
Acknowledgements. The present study was funded by the
Centre for Ecology & Hydrology Environmental Change
Integrating Fund project SPACE (Shifting Phenology:
Attributing Change across Ecosystems). SST data were pro-
vided courtesy of the NOAA National Oceanographic Data
Center and the University of Miami. We thank Mike Harris
and many others who collected seabird data, and all
past/present members and supporters of the Sir Alister
Hardy Foundation for Ocean Science for establishment and
maintenance of the CPR dataset and the owners and crews
of ships towing the CPRs. We are grateful to the Natural
Environmental Research Council and the Joint Nature Con-
servation Committee for supporting the long-term seabird
studies and to the Scottish Natural Heritage for allowing
work on the Isle of May. Five anonymous referees provided
constructive criticism which significantly improved the orig-
inal manuscript.
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... Although phenological mismatch is well studied, our understanding of its magnitude, impacts, and how it changes across scales remains limited. For example, there have been inconsistent findings on whether there are community-level phenological mismatches (Edwards and Richardson 2004;Donnelly et al. 2011;Burthe et al. 2012;Ovaskainen et al. 2013). Part of these inconsistencies arises from the different definitions and methods used to quantify phenological mismatch. ...
... Notably, this method allows the comparison of more than two species on the community level. Meta-analyses involving multiple taxa suggested differential phenological change among trophic levels (Edwards and Richardson 2004;Both et al. 2009;Thackeray et al. 2010;Burthe et al. 2012;Ovaskainen et al. 2013). The other change-based method is to compare the response in the timing of phenological events to an environmental change, i.e., comparing the sensitivity or slope of the regression line ( Fig. 1c[2]). ...
... Bloom timing of plankton has been correlated with sea bottom temperature (Koeller et al. 2009) and iceretreat timing (Ji et al. 2013). In a North Sea pelagic food web, the lack of significant correlations among species phenologies and with sea surface temperature were used as evidence of a trophic mismatch (Burthe et al. 2012). This method requires the assumption of a relatively tight linear coupling between variables. ...
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Context Climate change is driving phenological shifts across landscapes, but uncoordinated shifts might cause a potential “phenological mismatch.” There has been little consensus on the existence and magnitude of such a mismatch. The lack of agreement among studies can be attributed to the wide variety of definitions for the term “phenological mismatch,” as well as the methods used to measure it. The lack of comparability among measures of phenological mismatch creates a challenge for conservation. Objectives We proposed a novel theoretical framework to generalize existing measures of phenological mismatch and an approach to quantify the decoupling between phenology and the environment using the loss in predictive skill over time. We aimed to estimate the magnitude of phenological mismatch on large spatial scales and test the proposed predictive approach’s ability to detect multiple types of phenological mismatch. Methods We modeled historical climate-phenology coupling and quantified phenological mismatch as the deviation between observed and predicted phenology under climate change. First, we used two large empirical spatiotemporal datasets to estimate phenological mismatch in plant flowering phenology in the eastern United States and bird reproductive phenology in Finland. Historical climate-phenology coupling was modeled with spatial linear regression. Second, we conducted four simulation experiments representing different types of mismatch during climate change. We recovered simulated phenological mismatch by fitting a data-driven nonlinear model (Gaussian Process Empirical Dynamic Modeling) and predicting phenology. Results In the eastern US, we found that advancing plant flowering phenology generally matched spring warming from 1895 to 2015, with seven out of the 19 species studied having significant phenological mismatches, with observed flowering time earlier than predictions even considering warming. A similar phenological mismatch was found in birds in Finland from 1975 to 2017, with the bird breeding season advancing more than expected in 21 out of the 36 species studied. In four simulation experiments, we were able to accurately recover the simulated phenological mismatches in the timing of events, pace of development, and intensity of activities, although with greater challenges in quantifying a mismatch in life history. Conclusions Overall, these case studies show that our prediction-based measure effectively quantifies multiple types of phenological mismatch, providing a more generalizable and comparable measure of phenological mismatch across study systems and scales. This study will enable the investigation of phenological mismatch at large scales, improving understanding of the patterns and consequences of climate-change-induced phenological changes.
... Trophic mismatch can have variable impacts on predator populations, where predators may shift too slowly or rapidly in response to shifts in prey phenology (Burthe et al., 2012). These climatic driven changes have also resulted in the synchronization of once asynchronous resources, leading to prey-switching behavior among some predator populations (Deacy et al., 2017). ...
... Although mixed terrestrial and marine diets can facilitate weight gain in brown bears, older individuals with larger body masses can better maintain weight with increased lipid intake from salmon consumption, which likely contributed to their greater exploitation of salmon in our study (Costello et al., 2016). While negative effects of climate-induced phenological synchronization of food resources have occurred across diverse taxa (Burthe et al., 2012;Kerby and Post, 2013;, we did not find evidence of increased dietary switching to terrestrial resources in brown bears on the Kodiak Archipelago. Despite variation in the timings of food availability across and within years, salmon consumption remained high and appeared to reflect fluctuating salmon abundance into the system. ...
... Poor Lack of data on spatial and temporal variation in breeding timings between colonies (Burthe et al., 2012;Frederiksen et al., 2004a). Diet Moderate Some understanding of spatial variation in foraging behaviour and diet between colonies and regions during the breeding season, largely restricted to the North Sea (Johnston et al., 2021a). ...
Species face a multitude of stressors due to human activities, especially in marine environments. Seabirds are among the most threatened group of birds globally. A key challenge in their conservation is quantifying the impact of multiple interacting stressors on populations effectively, especially for species that undertake large-scale movements. We use the relatively well-studied Black-legged Kittiwake Rissa tridactyla as a case study to highlight knowledge gaps in demographic rates and how key stressors act on populations across different parts of their biogeographic range. From this starting point we provide a strategic approach to identify and prioritise data collection and research efforts from species and regions where data are currently lacking. Obtaining accurate and precise empirical data on demographic rates and movement will increase the pre-dictive accuracy, and realism, of population models, and confidence in how populations will respond to multiple stressors over the life and annual cycle, facilitating better management decisions.
... Evidence is mounting that the phenology of lower trophic levels (phytoplankton, zooplankton) is moving 5-10 days earlier per decade, faster and more consistently than higher trophic levels (adult fish, seabirds, marine reptiles and mammals) that are moving earlier by 0-2.5 days per decade 29 . This contrasting response could lead to trophic mismatch, whereby the timing of predators and their prey responds asynchronously to climate change 18 , with potential ecosystem consequences including poorer fish recruitment 111,112 , altered fish migration [113][114][115] and changes to the spawning of fish 116,117 , crabs and squid 118 . ...
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Zooplankton are major consumers of phytoplankton primary production in marine ecosystems. As such, they represent a critical link for energy and matter transfer between phytoplankton and bacterioplankton to higher trophic levels and play an important role in global biogeochemical cycles. In this Review, we discuss key responses of zooplankton to ocean warming, including shifts in phenology, range, and body size, and assess the implications to the biological carbon pump and interactions with higher trophic levels. Our synthesis highlights key knowledge gaps and geographic gaps in monitoring coverage that need to be urgently addressed. We also discuss an integrated sampling approach that combines traditional and novel techniques to improve zooplankton observation for the benefit of monitoring zooplankton popula- tions and modelling future scenarios under global changes.
... In some cases, different studies reported information on the same phenophase for the same species and location. Whenever the timespans of different studies did not fully overlap, we included in the database both pieces of information (e.g., Burthe et al., 2012;Frederiksen et al., 2004). Whenever the time series fully overlapped, we selected the longest one. ...
The alteration of the timing of biological events is one of the best documented effects of climate change, with overwhelming evidence across taxa. Many studies have investigated the phenology of consumers, especially birds. However, most of these studies have focused on specific phenophases, while a global analysis of avian phenological trends during recent climate change across different phases of the circannual cycle is still lacking. Here, we performed a comprehensive meta‐analytic synthesis of the phenological responses (temporal shifts in days year‐1) of birds across different phenophases (pre‐breeding migration, breeding, and post‐breeding migration) by summarizing more than 5500 time series from 684 species from five continents during 1811‐2018. Our results confirm that avian taxa have advanced pre‐breeding migration and breeding by ca. 2‐3 days per decade, while no significant temporal changes in the timing of post‐breeding migration were documented. Advancement in timing of pre‐breeding migration and breeding strongly depended on migratory behaviour, with the advance being the weakest for long‐distance migrants and the strongest for resident species. Diet generalists and primary consumers tended to advance pre‐breeding migration timing more than species with different dietary specializations. Increasing body size resulted in a larger advancement in the onset (but not in the mean date) of pre‐breeding migration and breeding, while phenological advances were larger in the northern than in the southern hemisphere. Our synthesis, covering most of the world, highlighted previously unappreciated patterns in avian phenological shifts over time, suggesting that specific life‐history or ecological traits may drive different responses to climate change.
... Around the globe, stories of environmental mismatches in timing are illustrating the complicated effects of climate change. In the Arctic, caribou may be arriving at their feeding grounds too late for peaks in new vegetation growth, with potentially devastating effects on new mothers and calves (Post and Forchhammer, 2008;Kerby and Post, 2013). 1 Atlantic puffins and European woodland birds may also be hatching chicks outside of the best times for catching prey (Burthe et al., 2012;Burgess et al., 2018). Worries about a 'time out of joint' apply not only to ecological contexts, but to social ones as well. ...
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Many scholars have argued that climate change is, in part, a problem of time, with ecological, political and social systems thought to be out of sync or mistimed. Discussions of time and environment are often interdisciplinary, necessitating a wide-ranging use of methods and approaches. However, to date there has been practically no direct engagement with the scientific field of phenology, the study of life-cycle timing across species, including plants, animals and insects. In this article, we outline how phenology can offer novel inroads to thinking through temporal relations across species and environments. We suggest that greater engagement with this field will enable scholars working across the humanities and social sciences to incorporate detailed studies of environmental timings which shed light on individual species, as well as wide-ranging species interactions. Following an overview of phenological research from both western scientific and indigenous knowledge perspectives, we report on a scoping exercise looking at where phenology has appeared in environmental humanities literature to date. We then offer an illustration that puts phenological perspectives into conversation with plant studies in order to indicate some of the useful affordances phenological perspectives offer, namely those of comprehending time as co-constructed across species and as flexible and responsive to environmental changes. We conclude by offering a number of further potential connections and suggestions for future research, including calling for more exploration of how environmental humanities approaches might produce critical contributions to phenology in their turn.
... Data such as those described in this paper are crucial in providing definitive answers as to why marine survival of Atlantic salmon continues to decline. The earlier return migration, coupled with smaller body size, point to several fruitful lines of investigation including: physiological challenges associated with growth rates (Tréhin et al., 2021;Vollset et al., 2022), changing ocean currents (Caesar et al., 2021), decreased feeding opportunities (Peyronnet et al., 2008;Utne et al., 2021) and trophic mismatches (e.g., Burthe et al., 2012). All of these potential causative agents are consistent with the impacts of anthropogenic climate change on the ocean, and are likely to interact in synergistic and antagonistic ways with Atlantic salmon stocks. ...
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Migration is an important ecological trait that allows animals to exploit resources in different habitats, obtaining extra energy for growth and reproduction. The phenology (or timing) of migration is a highly heritable trait, but is also controlled by environmental factors. Numerous studies have reported the advancement of species life-events with climate change, but the rate and significance of such advancement is likely to be species specific, spatially variable and dependent on interactions with population and ecosystem changes. This is particularly true for diadromous fishes which are sentinels of change in both freshwater and marine domains, and are subject to considerable multiple stressors including overfishing and habitat degradation. Here, we describe trends in the migration phenology of three native Irish migratory fishes over half a century, Atlantic salmon ( Salmo salar ), brown trout ( Salmo trutta ) and European eel ( Anguilla anguilla ). The trends were derived from daily counts of 745,263 fish moving upstream and downstream through the fish traps of the Burrishoole catchment, an internationally important monitoring infrastructure allowing a full census of migrating fish. We found that the start of the seaward migration of eel has advanced by one month since 1970. The commencement of the salmon smolt migration has advanced by one week, although the rest of the migration, and the entirety of the trout smolt run has remained stable. The beginning of the upstream migration of trout to freshwater has advanced by 20 days, while the end of the run is more than one month later than in the 1970’s. The greatest phenological shift has been in the upstream migration of adult salmon, with at least half of migrating fish returning between one and two months earlier from the marine environment compared to the 1970’s. The earlier return of these salmon is coincident with reduced marine survival and decreasing body size, indicating considerable oceanic challenges for this species. Our results demonstrate that the impacts of climate change on the phenology of diadromous fish are context-dependent and may interact with other factors. The mobilization of long-term datasets are crucial to parse the ecological impacts of climate change from other anthropogenic stresses.
Human activities have been exerting a non-negligible impact on aquatic environments globally, resulting in temperature rise, extreme weather events, acidification, and the emergence of hypoxic dead zones. Understanding how fish, the most diverse taxa in vertebrates, acclimate, adapt, survive, and sustain in this changing environment is of great importance for both the protection of diversity and aquatic production. Here, we summarize prominent issues concerning environmental stressors under global climate change and highlight the connections between fish responses and epigenetic modifications. Evidence suggests that epigenetic modifications play a role in almost all aspects of fish biology, e.g. sex determination and differentiation, gonadal development and reproduction, stress response and survival, growth, size and morphology, nutrition metabolism, etc. Therefore, epigenetic inheritance may play a significant role in fish acclimation and adaptation to climate change and in helping offspring cope with environmental stresses across generations. We finally present knowledge gaps in the connection between epigenetics and fish response to climate change, which will guide the priorities of future research work.
Climate warming can reduce food resources for animal populations. In species exhibiting parental care, parental effort is a ‘barometer’ of changes in environmental conditions. A key issue is the extent to which variation in parental effort can buffer demographic rates against environmental change. Seabirds breed in large, dense colonies and globally are major predators of small fish that are often sensitive to ocean warming. We explored the causes and consequences of annual variation in parental effort as indicated by standardised checks of the proportions of chicks attended by both, one or neither parent, in a population of common guillemots Uria aalge over four decades during which there was marked variation in marine climate and chick diet. We predicted that, for parental effort to be an effective buffer, there would be a link between environmental conditions and parental effort, but not between parental effort and demographic rates. Environmental conditions influenced multiple aspects of the prey delivered by parents to their chicks with prey species, length and energy density all influenced by spring sea surface temperature (sSST) in the current and/or previous year. Overall, the mean annual daily energy intake of chicks declined significantly when sSST in the current year was higher. In accordance with our first prediction, we found that parental effort increased with sSST in the current and previous year. However, the increase was insufficient to maintain chick daily energy intake. In contrast to our second prediction, we found that increased parental effort had major demographic consequences such that growth rate and fledging success of chicks, and body mass and overwinter survival of breeding adults all decreased significantly. Common guillemot parents were unable to compensate effectively for temperature‐mediated variation in feeding conditions through behavioural flexibility, resulting in immediate consequences for breeding population size because of lower adult survival and potentially longer‐term impacts on recruitment because of lower productivity. These findings highlight that a critical issue for species' responses to future climate change will be the extent to which behavioural buffering can offer resilience to deteriorating environmental conditions.
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Climate change has led to widespread shifts in the timing of key life history events between interacting species (phenological asynchrony) with hypothesized cascading negative fitness impacts on one or more of the interacting species—often termed ‘mismatch’. Yet, predicting the types of systems prone to mismatch remains a major hurdle. Recent reviews have argued that many studies do not provide strong evidence of the underlying match‐mismatch hypothesis, but none have quantitatively analysed support for it. Here, we test the hypothesis by estimating the prevalence of mismatch across antagonistic trophic interactions in terrestrial systems and then examine whether studies that meet the assumptions of the hypothesis are more likely to find a mismatch. Despite a large range of synchrony to asynchrony, we did not find general support for the hypothesis. Our results thus question the general applicability of this hypothesis in terrestrial systems, but they also suggest specific types of data missing to robustly refute it. We highlight the critical need to define resource seasonality and the window of ‘match’ for the most rigorous tests of the hypothesis. Such efforts are necessary if we want to predict systems where mismatches are likely to occur.
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The lesser sandeel Ammodytes marinus is a key species in the North Sea ecosystem, transferring energy from planktonic producers to top predators. Previous studies have shown a long-term decline in the size of 0-group sandeels in the western North Sea, but they were unable to pinpoint the mechanism (later hatching, slower growth or changes in size-dependent mortality) or cause. To investigate the first 2 possibilities we combined 2 independent time series of sandeel size, namely data from chick-feeding Atlantic puffins Fratercula arctica and from the Continuous Plankton Recorder (CPR), in a novel statistical model implemented using Markov Chain Monte Carlo (MCMC). The model estimated annual mean length on 1 July, as well as hatching date and growth rate for sandeels from 1973 to 2006. Mean length-at-date declined by 22% over this period, corresponding to a 60% decrease in energy content, with a sharper decline since 2002. Up to the mid-1990s, the decline was associated with a trend towards later hatching. Subsequently, hatching became earlier again, and the continued trend towards smaller size appears to have been driven by lower growth rates, particularly in the most recent years, although we could not rule out changes in size-dependent mortality. Our findings point to major changes in key aspects of sandeel life history, which we consider are most likely due to direct and indirect temperature-related changes over a range of biotic factors, including the seasonal distribution of copepods and intra- and inter-specific competition with planktivorous fish. The results have implications both for the many predators of sandeels and for age and size of maturation in this aggregation of North Sea sandeels.
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We show that the distributions of both exploited and nonexploited North Sea fishes have responded markedly to recent increases in sea temperature, with nearly two-thirds of species shifting in mean latitude or depth or both over 25 years. For species with northerly or southerly range margins in the North Sea, half have shown boundary shifts with warming, and all but one shifted northward. Species with shifting distributions have faster life cycles and smaller body sizes than nonshifting species. Further temperature rises are likely to have profound impacts on commercial fisheries through continued shifts in distribution and alterations in community interactions.
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Sandeels Ammodytes marinus are important food for many breeding seabirds in the North Sea, and are harvested in large quantities by an industrial fishery. There is very little evidence of the fishery reducing availability of sandeels to breeding seabirds, but there is concern that fishery managers should take account of the needs of breeding seabirds. Here we present a quantitative index of the sensitivity of different seabird species' breeding success to reduced abundance of sandeels. The index is based on seabird size, cost of foraging, potential foraging range, ability to dive, amount of 'spare' time in the daily budget, and ability to switch diet. Testing the index with empirical data from Shetland during periods of reduced sandeel abundance shows a close correlation between seabird breeding performance and predictions from the index. Mapping the distributions around the North Sea of seabirds with breeding success highly sensitive to sandeel abundance shows that the majority of sensitive seabirds breed in Shetland and Orkney. industrial fishing in those regions should be closely controlled to avoid depleting the local sandeel stocks on which seabirds depend. This analysis considers only impacts on seabird breeding. There is a need for analysis of possible influences on other aspects of seabird demography.
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Spatial and temporal patterns of Calanus finmarchicus and C. helgolandicus (Copepoda, Calanoida) were investigated in the northeast Atlantic and the North Sea from 1962 to 1992. The seasonal cycle of C. finmarchicus is characterised by a single peak of abundance in spring, whereas the seasonal cycle of C. helgolandicus shows 2 abundance maxima, one in spring and one in autumn. The former species mainly occurs in northern regions (limited by the 55 degrees N parallel in the North Sea and by the 50 degrees N parallel in the open ocean). The latter species shows 2 types of spatial patterns, occurring in the Celtic Sea during spring and in the Celtic Sea plus the North Sea in autumn. Differences in seasonal spatial patterns of Calanus species may result from different responses to the environment, ultimately due to different life cycle strategies, different vertical distributions, opposite temperature affinities and interspecific competition. Futhermore, results reveal that annual means of abundance are closely related to annual maxima and to spatial extensions of the species. It also appears that the long-term trends of the 2 Calanus species are opposite: C. finmarchicus shows a clear downward trend in abundance, while C. helgolandicus presents an upward one.
The common approach to the multiplicity problem calls for controlling the familywise error rate (FWER). This approach, though, has faults, and we point out a few. A different approach to problems of multiple significance testing is presented. It calls for controlling the expected proportion of falsely rejected hypotheses — the false discovery rate. This error rate is equivalent to the FWER when all hypotheses are true but is smaller otherwise. Therefore, in problems where the control of the false discovery rate rather than that of the FWER is desired, there is potential for a gain in power. A simple sequential Bonferronitype procedure is proved to control the false discovery rate for independent test statistics, and a simulation study shows that the gain in power is substantial. The use of the new procedure and the appropriateness of the criterion are illustrated with examples.
The degree of match and mismatch in the time of larval production and production of their food has been put forward as an explanation of part of the variability in recruitment to a stock of fish. The magnitude of recruitment is not completely determined until the year-class finally joins the adult stock, and the processes involved probably begin early in the life-history of the fish when both their growth and mortality rates are high. The match/mismatch hypothesis is given in this chapter to cover the subsequent development through larval life up to metamorphosis, and possibly just beyond. The match/mismatch hypothesis has now been extended to the upwelling areas and oceanic divergences equatorward of 40° latitude on the basis that fish in these regions release batches of eggs more frequently when they are well fed and, more generally, that pelagic fish may modify their reproductive strategies such that they can feed and spawn at the same time. A delay in predation is of great importance, particularly when production peaks in early development. This model illustrates the difficulties that occur when growth and mortality are allowed to interact. On the other hand, there are three consequences of the match/mismatch hypothesis that are presented in this chapter. However, the limited conclusion drawn in this chapter is that, investigations of fish larvae should continue to be a part of the study of population dynamics of fishes.