Body size-dependent responses of a marine fish assemblage ...

Body size-dependent responses of a marine fishassemblage to climate change and fishing over acentury-long scale

M A R T I N J . G E N N E R *w , D AV I D W. S I M S *z, A L A N J . S O U T H WA R D *{ ,

G E O R G I N A C . B U D D *, PA T R I C I A M A S T E R S O N *, M A T T H E W M C H U G H *,

P E T E R R E N D L E *, E M I LY J . S O U T H A L L *, V I C T O R I A J . W E A R M O U T H * and

S T E P H E N J . H A W K I N S *§

*Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK, wSchool of Biological

Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK, zMarine Biology and Ecology Research Centre, School of

Biological Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK, §College of Natural Sciences, Memorial

Building, Bangor University, Gwynedd LL57 2UW, UK

Abstract

Commercial fishing and climate change have influenced the composition of marine fishassemblages worldwide, but we require a better understanding of their relative influence onlong-term changes in species abundance and body-size distributions. In this study, weinvestigated long-term (1911–2007) variability within a demersal fish assemblage in thewestern English Channel. The region has been subject to commercial fisheries throughoutmost of the past century, and has undergone interannual changes in sea temperature of over2.0 1C. We focussed on a core 30 species that comprised 99% of total individuals sampled in theassemblage. Analyses showed that temporal trends in the abundance of smaller multispeciessize classes followed thermal regime changes, but that there were persistent declines inabundance of larger size classes. Consistent with these results, larger-growing individualspecies had the greatest declines in body size, and the most constant declines in abundance,while abundance changes of smaller-growing species were more closely linked to precedingsea temperatures. Together these analyses are suggestive of dichotomous size-dependentresponses of species to long-term climate change and commercial fishing over a century scale.Small species had rapid responses to the prevailing thermal environment, suggesting theirlife history traits predisposed populations to respond quickly to changing climates. Largerspecies declined in abundance and size, reflecting expectations from sustained size-selectiveoverharvesting. These results demonstrate the importance of considering species traits whendeveloping indicators of human and climatic impacts on marine fauna.

Keywords: climate change, fisheries, life history traits, marine monitoring, overfishing

Received 9 February 2009; revised version received 21 June 2009 and accepted 29 June 2009

Introduction

Striking ecosystem-level changes have taken place in

marine coastal environments over the last century

through both natural and anthropogenic causes.

Commercial fishing has influenced the abundance of

many target marine fish species, with evidence from

both long-term monitoring and contemporary resur-

veys of sites for which historic datasets are avail-

able (Jennings & Kaiser, 1998; Jackson et al., 2001).

Although many fisheries are stable or recovering, sus-

tained fishing has negatively influenced the reproduc-

tive capacity of many populations, even to the extent

that a small number of formerly abundant marine

species are now economically or biologically extinct

(Reynolds et al., 2005). Fisheries target larger indivi-

duals within populations, often from slow-growing,

late-maturing and long-lived species that produce few

offspring (Jennings et al., 1999). As a consequence of

these life-history traits commercial target species can be

the least resilient to chronic fishing pressure (Jennings &

Kaiser, 1998). Importantly, such species are often top

Correspondence: M. J. Genner, School of Biological Sciences,

University of Bristol, Woodland Road, Bristol BS8 1UG, UK,

tel. 1 44 117 928 9827, fax 1 44 117 331 7985, e-mail:

[email protected]

{Deceased 27 October 2007.

Global Change Biology (2009), doi: 10.1111/j.1365-2486.2009.02027.x

r 2009 Blackwell Publishing Ltd 1

mailto:[email protected]

predators and their overharvesting can have broader

ecosystem-level implications, including cascading den-

sity-dependent effects on other trophic levels (Frank

et al., 2005; Myers et al., 2007).

In northern European waters commercial bottom-

trawl fisheries have operated since the late 18th century,

but marine fisheries using static gears such as long-lines

and fixed nets date back to medieval times (Barrett et al.,

2004). Industrialization and technological development

of fisheries in the region over the 20th century has led to

the increased concerns about the resilience of fished

stocks (Sims & Southward, 2006). Evidence of the

negative effects of unsustainably high fishing activity

is available for many regional stocks, including those

species with key commercial and ecological importance,

most notably Atlantic cod (Gadus morhua) (Cook et al.,

1997). Moreover, overfishing has been linked to the

regional extirpation of several other large-bodied de-

mersal species with less commercial importance includ-

ing common skate (Dipturus batis) from the Irish Sea

(Brander, 1981), and angel shark (Squatina squatina)

from the English Channel (Rogers & Ellis, 2000; Dulvy

et al., 2003).

Although the effects of fishing are pronounced, cli-

matic shifts have also been implicated as major causes

of fluctuations in marine fish diversity and abundance

in both pelagic and demersal assemblages (Alheit &

Hagen, 1997; Genner et al., 2004; Lehodey et al., 2006;

Hiddink & ter Hofstede, 2008). Long-term changes in

climate have been related to changes in recruitment

(Beaugrand et al., 2003), growth (Thresher et al., 2007),

migration phenology (Sims et al., 2004), depth distribu-

tions (Dulvy et al., 2008) and latitudinal distributions

(Perry et al., 2005). Given the consistent warming of

North Atlantic sea surface temperatures (SST) since the

mid-1980s (Mackenzie & Schiedek, 2007) and recent

predictions of a 0.5–4 1C increase over the next century

(Sheppard, 2004), there is a need to identify which

species are most likely to respond to climate change,

the nature of that response, and the timescales over

which this will take place. This is not least because

climate change effects have been suggested to have a

role in causing fish population declines (Schiermeier,

2004), in addition to well-documented widespread and

long-lasting declines due to overfishing (Jackson et al.,

2001).

Here, we examined changes in abundance and body

size within a demersal fish assemblage from the inshore

waters of the English Channel over a 97-year period

(1911–2007). This site contains a diverse fauna of south-

ern and northern-distributed fish species, with poten-

tially contrasting responses to climate and other factors

(Southward et al., 1995, 2005; Hawkins et al., 2003). We

used these data to first investigate long-term changes in

the abundance of size classes within the assemblage. We

then tested if larger-bodied species in the assemblage

have shown declines in abundance and body size over

the period, consistent with overfishing. We next tested if

smaller-bodied fish species, given their intrinsic poten-

tial for greater population growth (Denney et al., 2002),

and their known responses to climate in the North Sea

(Hiddink & ter Hofstede, 2008), have shown more

pronounced abundance responses to favourable cli-

matic conditions. Finally, we tested whether small and

large-bodied components of the species assemblage

have undergone parallel or contrasting long-term pat-

terns of structural change.

Materials and methods

Survey site and data collection

In total 1020 otter trawls were undertaken at 30–50 m

depth over a spatial scale of 51� 22 km (501080–501200N,

31550–041390W; Fig. S1) during 48 years from 1911 to

2007 (1911, 1913–14, 1919–22, 1950–58, 1967–79, 1983–94,

2001–07; Table S1). Abundance of 74 demersal fish taxa

were recorded, and of these five were treated as multi-

species groups, because records did not always identify

individuals to species. For brevity, each of these multi-

species groups (Table S2) is henceforth referred to as

one species. Pelagic taxa were excluded from analyses

as they were not recorded in all sampling years. Seven

vessels were used for sampling, ranging in overall

length from 18.3 to 39.0 m. Where data are available,

trawls were undertaken at the same speeds and were

comparable in dimensions: headline length range,

16.2–19.8 m; groundrope length range, 19.8–27.4 m;

main net stretched mesh diameter, 75–270 mm, and all

vessels used a fine-mesh cod end or a cover (Table S3).

The data analysed here are independent of commercial

landings and are not confounded by changes in fishing

practices, market forces or quota restrictions. The sur-

vey gears ensured that small noncommercial species

were sampled, species that would pass through the

wider mesh of commercial gears. The median number

of hauls per year was 16 (range 1–98), and the median

duration of each haul of the trawl was 60 min (range

8–210). Length data were collected during 1911,

1919–22, 1950–57, 1979–1986 and 2001–2007. Typically

in hauls where length data were collected, all indivi-

duals were measured, except when species were very

abundant which necessitated subsampling. Since 1911,

between 72 and 13 440 individuals have been measured

per species used in the analyses (Table S4). Mass data

were collected from measured specimens between 2001

and 2007.

2 M . J . G E N N E R et al.

r 2009 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2009.02027.x

Environmental data

SST data were derived from the Global Ocean Surface

Temperature (GISST) databank of the UK Meteorologi-

cal Office Hadley Centre via the British Atmospheric

Data Centre (http://badc.nerc.ac.uk). Data comprise

monthly means for 11 latitude and longitude units

dating back to 1871. Over the last century there have

been notable changes in SST of the English Channel:

following a cold period during the 1910s and 1920s

there was a rise in SST towards the 1950s, a slight

cooling from the 1960s to the early 1980s, and a rapid

warming since the mid-1980s (Southward et al., 2005).

These trends were most prominent in winter measure-

ments (Fig. 1a and b), and similar trends in SST have

taken place throughout the North-East Atlantic (Shep-

pard, 2004). In the sampling region, SST accurately

reflects bottom temperatures in winter; in summer the

waters are stratified leading to surface waters � 4 1C

warmer. To provide an indication of consistency of

fishing activity in the region, data on landings by area

of capture were collated from UK government records

(Fig 1c and d). Given mortality data for the assemblage

are largely absent, no attempts were made to derive

direct associations between fisheries effort and long-

term change in our focal assemblage.

Identification of core species in the assemblage

Temporal trends of rarer species can be difficult to

quantify accurately from trawl survey data. Thus, we

only examined abundance changes in common or ‘core’

species with the highest incidence (number of years

present in the dataset) over the sampling period. The 30

core species comprised 99.1% of the estimated 987 305

individuals sampled between 1911 and 2007.

Temporal change in abundance of size-classes in the corespecies assemblage

We used the survey data to explore temporal change

in mean annual catch per unit effort (CPUE) of indivi-

7.5

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1910 1930 1950 1970 1990 2010Year

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n se

a su

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mpe

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reJu

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C)

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n se

a su

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y–M

arch

(°C

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Fig. 1 Mean (a) winter and (b) summer sea surface temperature (SST) 1910–2007 off Plymouth (grid square (50–511N, 04–051W). Data

from the UK Meteorological Office Hadley Centre, 5-year running means include the focal year and previous 4 years. For illustrative

purposes only, (c) UK fleet demersal fish landings from the English Channel (ICES areas VIId/e), and (d) landings at the port of

Plymouth. Data from UK Government Fisheries Statistics; grey areas indicate war years.

C L I M AT E , F I S H I N G A N D M A R I N E F I S H A S S E M B L A G E S 3


http://badc.nerc.ac.uk























duals in multispecies size categories within the core

assemblage. We calculated the mean annual CPUE

(individuals caught per hour trawling) of each core

species across all hauls in the year. For each species

during each of these years we then calculated the

proportion of all sampled individuals belonging to each

size class, and multiplied these by the mean annual

species CPUE. This enabled us to calculate mean annual

CPUE of each multispecies size class. Substantial varia-

tion in body shape among sampled species is likely to

have influenced relative vulnerability to commercial

fishing gears, thus consideration of both mass and

length parameters is valuable. Since only total length

was available before 2001, we estimated individual

mass using species length–weight relationships derived

from specimens sampled for both parameters since 2001

(Table S4). Although these relationships may have

varied in the sampling area over time, we assume

variation would ensure only marginal influence on

larger-scale patterns in our results. We identified the

most likely drivers of variation in CPUE (log10[x 1 1]

transformed) of the smallest size category using multi-

ple regression, employing as predictor variables the

mean winter (January–March) SST for the focal and

previous year and the mean summer (July–September)

SST for the focal and previous year, as indicators of

climatic variability. We also included CPUE (log10[x 1 1]

transformed) of fish in the two largest size categories,

representing abundance of potential predators.

Changes in body size of species

As an index of the change in body size of sampled

individuals within each species over time, we measured

the slope of linear relationships between sampling year

and body size of all sampled individuals. Spearman’s

rank correlations (rs) were used to test for significant

cross-species associations between body size changes

and maximum species body sizes early in the time

series (1911–22), namely maximum total length (Lmax)

and maximum mass (Wmax).

Changes in abundance of species

As an index of change in abundance of core species

from 1911 to 2007 we used Pearson’s correlation coeffi-

cient (r) of log10(x 1 1) transformed mean annual CPUE

against year. As an index of climate-related change in

abundance of core species from 1911 to 2007 we used

Pearson’s correlation coefficient of log10(x 1 1) trans-

formed mean annual CPUE since 1911 against SST,

making the assumption of linearity of species re-

sponses. Correlation coefficients were used to quantify

abundance trends in preference to slope coefficients due

to their lack of dependence on average species abun-

dance across all sampling years. Multiple regression

was used to test for associations between abundance

trends, maximum body size, and northerly limits of

species distributions. Distributional data were sourced

from Fishbase (Froese & Pauly, 2008).

Size-dependent patterns of assemblage structural change

We divided the 30 core species into larger and small

species based on maximum body mass of individuals

sampled in 1911–1922 (large species Wmax4900 g; Table

S4). A matrix of quarterly average catch per hour for

each species (rows: year quarter; columns: species) was

calculated, and data for each species were log10(x 1 1)

transformed and standardized (mean 5 0; SD 5 1). To

condense multivariate variability into fewer dimensions

we used principal component analysis (PCA) on the

derived correlation matrix of Primer-6 (Primer-E Ltd,

Plymouth, UK). This enabled us to identify prominent

patterns of temporal structural change in the multivari-

ate data. Species contributing strongly to principal com-

ponent axis 1 (PC1), the primary descriptor of change,

were identified for descriptive purposes as those with

loadings 40.4 or o�0.4. Multiple regressions were used

to test for dependence of PC1 on sea temperatures.

Results

Abundance of size classes

Individuals in the 0–200 mm and 0–200 g size categories

increased in abundance towards the 1950s, declined

towards the 1980s and increased from the late 1980s

onwards. Medium sized fishes in the 201–800 mm and

201–1600 g size categories gradually increased in abun-

dance throughout the time series. By contrast large

fishes 4801 mm and 41601 g declined in abundance

(Fig. 2). Small species dominated the assemblage by

number, with species o200 g comprising on average

87.4% (range 64–99%) of the core assemblage, and

species o200 mm on average comprising 63.3% (range

13.2–92.9%). In multiple regression analyses, log-trans-

formed abundance of smallest size categories was sig-

nificantly dependent on winter SSTs of the focal and

previous years (Table 1).

Body size as a predictor of abundance and size changes

Species with greater maximum body size declined most

consistently in abundance over the sampling period

(Fig. 3a and b), while species with smaller body size

were more strongly associated with climatic variability

(Fig. 3d and e). Northerly limits were not significant



predictors of abundance trends, or associations with

climatic variability (Fig. 3c and f). Although larger bod-

ied species had more extensive northerly limits, associa-

tions were not significant (Fig. 3i). In multiple regression

analyses, maximum body mass was consistently the best

predictor of responses to climatic variability (Table 2).

Species with larger body size declined the most in size

over the time series (Table 2; Fig. 3g and h), most notably

Atlantic cod, anglerfish (Lophius piscatorius), ling (Molva

molva), pollock (Pollachius pollachius), turbot (Scophthal-

mus maximus) and rays (Table S5). Across all response

variables, maximum body mass was the most effective

predictor of species change (Table 2; Fig. 3).

Changes in assemblage structure

In the species subset with smaller body size, PC1

captured 29.49% of the variation and interannual varia-

tion was greater than observed seasonal variation (Fig.

4a). In multiple regression analyses mean annual PC1

was significantly positively associated with winter SST

for the focal and previous years (Table 3). Species

strongly associated with this axis were solenette

(Buglossidium luteum), common dragonet (Callionymus

lyra), red bandfish (Cepola macrophthalma), grey gurnard

(Eutrigla gurnardus), whiting (Merlangius merlangus),

thickback sole (Microchirus variegatus), red mullet (Mullus

0 – 200 mm

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4

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nual

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indi

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, log

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0 – 200 g

Fig. 2 Temporal change in abundance of individuals in length and mass classes within the core assemblage.



surmuletus), topknots (Phrynorhombus sp.) and poor cod

(Trisopterus minutus); all increased in abundance with

warming waters (Table S5).

In the species subset with larger body size, PC1

captured 17.09% of the variation and interannual varia-

tion was greater than observed seasonal variation (Fig.

4b). Mean annual PC1 of the larger species showed a

similar pattern to the smaller species subset until the

late 1970s and early 1980s when demersal landings

from commercial fisheries in the region increased three-

fold (Fig. 2c). After this period, while smaller species

continued to track climate-forced SST variability, larger

species showed an opposing trend. The species with the

strongest loadings on this axis declined in abundance

after the 1950s, including conger eel (Conger conger),

anglerfish (Lophius sp.), hake (Merluccius merluccius),

rays (Rajiidae), brill (Scophthalmus rhombus) and Dover

sole (Solea solea) (Table S5). Mean annual PC1 of the

large species was not significantly associated with any

tested SST variables (Table 3), or mean annual PC1 of

small species (r 5�0.224, n 5 48, P 5 0.126).

Discussion

Here, we present evidence of 97 years of change in a

local marine fish assemblage in the Western English

Channel. We observed declines in both the abundance

and size distribution of larger species, to the extent that

in the largest mass category (43200 g) there was a 91%

decrease in mean catch rates, from 1.84 individuals per

hour in 1911–22 to 0.09 individuals per hour in 2001–

2007. Truncation of the size-structure of target popula-

tions is one of the most commonly observed effects of

commercial trawling due to the intrinsically size-selec-

tive nature of bottom trawls (Froese, 2004). Negative

size-shifts can impede the maintenance and recovery of

exploited marine fish populations because larger indi-

viduals are typically the most fecund, and their sus-

tained removal can severely reduce average individual

lifetime egg production in the population (O’Farrell &

Botsford, 2006). This effect can be compounded in

broadcast-spawning species where several years of

poor recruitment often occur before favourable envir-

onmental conditions prevail. Our analyses demonstrat-

ing both greater declines in abundance of larger species,

and truncations of size distributions, are consistent with

the cumulative effects of over a century of commercial

fisheries operating in the region (Fig. 1c and d). Other

heavily fished habitats ranging from temperate conti-

nental shelves (Blanchard et al., 2005; Levin et al., 2006)

to coral reefs (Dulvy et al., 2004; Graham et al., 2005) and

the open oceans (Ward & Myers, 2005) show similar

patterns. However, identifying the relative signals of

climate change and fishing within a single assemblage

has not been routinely undertaken.

It should be considered whether declines in abun-

dance and size-distributions of larger species reflect a

fundamental long-term shift in their distributions, per-

haps due to northwards biogeographic shifts. There is

some evidence that biogeographical shifts have oc-

curred in northern European waters, for example cod

within the North Sea (Perry et al., 2005). However, the

declines in abundance and size distribution in our

study are not exclusively in northern species. We ob-

served overall declines in rays, most of the species of

which that were found in our surveys (Table S2) have

broad distributions including the Bay of Biscay and the

Mediterranean. Similar patterns were found in the south-

Table 1 Multiple regressions of CPUE of the smallest size classes against SST and CPUE of larger size classes

Response Predictor Slope SE t P

Mean annual abundance

(CPUE) individuals

o200 mm length

Constant �1.709 0.102

CPUE individuals 801–1000 mm �0.160 0.173 �0.921 0.367

CPUE individuals 1001 1 mm �0.047 0.158 �0.297 0.769

Winter SST focal year 0.586 0.164 3.557 0.001

Winter SST 1-year lag 0.356 0.171 2.073 0.050

Summer SST focal year �0.148 0.158 �0.933 0.360

Summer SST 1-year lag �0.160 0.173 �1.709 0.102

Mean annual abundance

(CPUE) individuals

o200 g mass

Constant �1.667 0.110

CPUE individuals 1600–3200 g 0.060 0.184 0.328 0.745

CPUE individuals 3201 1 g �0.127 0.200 �0.633 0.533




Summer SST 1-year lag �0.057 0.161 �0.357 0.724

Final models: CPUE o200 mm length (r2 5 0.671, F6, 21 5 7.124, Po0.001); CPUE o200 g mass (r2 5 0.648, F6, 21 5 6.451, Po0.001).

SST, sea surface temperature.



erly distributed hake, conger eel and anglerfish. Together

this suggests that thermal tolerances alone do not fully

explain the changes in abundance and size distributions

observed among the larger species within the assemblage.

Additionally, in the North Sea rising sea temperatures

have been shown to influence the depth distributions of

species (Dulvy et al., 2008). The limited spatial scale of our

study means we cannot assess the possibility that depth

shifts have altered the relative abundance of species.

Nevertheless, analyses of spatially explicit International

Bottom Trawl Survey data from the English Channel and

Celtic Sea areas may help reveal if changes in depth

distributions have taken place in the region.

Our results showed SSTs during the focal and pre-

ceding years were significant predictors of abundance

of small individuals in the core assemblage, a size class

dominated by species with short life histories. However,

the effect was not observed in the large species, sug-

gesting that climatic influences have not had an over-

riding influence on abundance of larger taxa within the

study location during the data collection period. This

may be because smaller marine fish species have in-

trinsically higher potential population growth rates

(Denney et al., 2002), and thus may have the capacity

to respond more rapidly to favourable climatic regimes.

There are several potential but nonmutually exclusive

mechanisms by which favourable climate may have

influenced the abundance of small fishes. Warmer

waters can enable shifts in distributions to waters in

which they were previously thermally excluded, or

alternatively, in range-restricted local populations rapid

abundance changes may result from climate influences

on survivorship in overwintering habitat. Our analyses,

necessarily based on data conducted over a limited

–0.8

0

0.4

0.8(a) (b) (c)

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Abu

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CP

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(d)

(g)

(e)

(h)

(f)

(i)

0

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Clim

ate

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ST

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2 2.2 2.4 2.6 2.8 3 3.2 3.4 1 2 3 4 5 50 55 60 65 70 75 80 85

Clim

ate

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ion

(cor

rela

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CP

UE

× w

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r S

ST

foca

l yea

r)

–5

–4

–3

–2

–1

0

1

2

–60

–50

–40

–30

–20

–10

0

10

1

2

3

4

Maximum length (log mm) Maximum mass (log g)

Leng

th c

hang

e (m

m y

r )

5

2 2.2 2.4 2.6 2.8 3 3.2 3.4 1 2 3 4 5 50 55 60 65 70 75 80 85

Northerly biogeographic limit (°N)

Max

imum

mas

s (lo

g

g)

Mas

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(g

yr

)C

limat

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soci

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E ×

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T fo

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× y

ear)

Fig. 3 Associations over the study period (1911–2007) between (a) species Lmax and abundance trend (r2 5 0.082, F1, 28 5 2.499,

P 5 0.125); (b) species Wmax and abundance trend (r2 5 0.151, F1, 28 5 4.996, P 5 0.034); (c) species northerly biogeographic limit and

abundance trend (r2 5 0.018, F1, 28 5 0.504, P 5 0.484); (d) species Lmax and absolute abundance association with winter SST (r2 5 0.400,

F1, 28 5 18.639, Po0.001); (e) species Wmax and absolute abundance association with winter SST (r2 5 0.385, F1, 28 5 17.601, Po0.001); (f)

species northerly limit and abundance association with winter SST (r2 5 0.14, F1, 28 5 4.59, P 5 0.41); (g) species Lmax and slope of body

length 1911–2007 (rs 5�0.241, P 5 0.204); (h) species Wmax and slope of body mass 1911–2007 (rs 5�0.374, P 5 0.041); (i) species body size

and northerly biogeographic limits. (Lmax r 5 0.355 P 5 0.054; Wmax, r 5 0.3270 P 5 0.078; i).



spatial scale, cannot directly test these possibilities.

Nevertheless, the presence of species showing rapid

positive responses to climatic warming during the cool-

er climatic periods suggests complete thermal exclusion

had not taken place. Since many of the small species

with the strongest linear associations with climate

change were more characteristic of southern Lusitanian

fauna, warmer waters may have reduced overwintering

mortality rates. This could have been directly through

reduced thermal physiological stress and faster growth

rates, or indirectly through enhanced prey availability

and reduced vulnerability to predators by thermal

influences on behaviour (Hurst, 2007). These results

imply a significant component of bottom-up forcing of

the Western English Channel fish community structure,

consistent with modelling results from this ecosystem

(Araujo et al., 2006).

Many of the larger species in our study area are

piscivorous top predators that exert influence on abun-

dance of prey populations, and it is possible that

removal of these ecologically important fish may have

released the smaller section of the assemblage from top-

down control and resulted in the observed rapid shifts

in relation to climatic variability. If the observed pat-

terns are primarily linked to predator release, we might

have expected numbers of small species to be low

during the 1950s when numbers of larger species were

higher in the post-war period of the 1950s. However,

evidence of relatively high abundance of both small and

large species in the 1950s provides evidence that release

from top-down control by predators has not been the

primary driver of abundance trends in the smaller

species. Instead, our results are more consistent with

climatic changes forcing long-term abundance fluctua-

tions in the noncommercial component of the assem-

blage, through distributional and/or population size

changes. The reason for the absence of detectable posi-

tive responses of most larger-bodied species to warmer

temperatures is unclear, but it is unlikely to be linked to

thermal preference alone. More likely explanations are

that either sustained removal of the spawning stock

biomass of large species may have constrained the

ability of larger fish to respond to favourable environ-

mental regimes, despite the potential for additional

trophic resources to enhance growth and greater re-

cruitment, or that numbers are now too low in our

dataset to provide the statistical power required to

detect responses to climatic variability. Some evidence

Table 2 Multiple regressions of abundance responses of core species in the assemblage against body size

Response Predictor Slope SE t P

(i) Abundance change (1911–2007) Constant �1.013 0.320

Lmax (1911–22) 1.100 0.601 1.830 0.079

Wmax (1911–22) �1.416 0.595 �2.382 0.025

Northern limit �0.083 0.182 �0.457 0.651

(ii) Abundance change (1950–2007) Constant �0.801 0.430

Lmax (1911–22) 0.839 0.594 1.412 0.170

Wmax (1911–22) �1.255 0.588 �2.134 0.042

Northern limit �0.021 0.180 �0.116 0.909

(iii) Climate association (1911–2007) (winter SST focal year) Constant �0.626 0.537

Lmax (1911–22) 1.249 0.468 2.666 0.013

Wmax (1911–22) �1.736 0.463 �3.746 0.001

Northern limit �0.252 0.142 �1.773 0.088

(iv) Climate association (1911–2007) (winter SST lagged 1 year) Constant �0.218 0.829

Lmax (1911–22) 1.051 0.501 2.099 0.046

Wmax (1911–22) �1.519 0.495 �3.068 0.005

Northern limit �0.252 0.152 �1.665 0.108

(v) Climate association (1911–2007) (summer SST focal year) Constant �1.023 0.316

Lmax (1911–22) 1.439 0.530 2.715 0.012

Wmax (1911–22) �1.746 0.524 �3.330 0.003

Northern limit �0.280 0.161 �1.746 0.093

(vi) Climate association (1911–2007) (summer SST lagged 1 year) Constant �0.226 0.823

Lmax (1911–22) 1.031 0.522 1.976 0.059

Wmax (1911–22) �1.462 0.516 �2.831 0.009

Northern limit �0.256 0.158 �1.621 0.117

Final models: (i) r2 5 0.249, F(3, 26) 5 2.875, P 5 0.055; (ii) r2 5 0.265, F(3, 26) 5 3.138, P 5 0.042; (iii) r2 5 0.543, F(3, 26) 5 10.334, Po0.001;

(iv) r2 5 0.479, F(3, 26) 5 7.964, Po0.001; (v) r2 5 0.416, F(3, 26) 5 6.179, P 5 0.003; (vi) r2 5 0.433, F(3, 26) 5 6.642, P 5 0.002.

SST, sea surface temperature.



supports these explanations; the only large species in

the core assemblage showing consistent abundance

increases with the warming climate was lesser-spotted

dogfish (Table S5), an elasmobranch with little commer-

cial value that is usually discarded by fishers, exhibits

high survivorship and can be caught in high abundance

(Revill et al., 2005).

It is important to consider other potential causes of

change in this marine fish assemblage. Many marine

inshore habitats have been affected by other human

activities, including discharge of pollutants, eutrophica-

tion and marine aquaculture, and there is evidence to

suggest that these have strongly impacted many regio-

nal fisheries based on marine and anadromous species

of inshore and estuarine habitats. However, such

changes are unlikely to have been driving the observed

long-term changes that have taken place in our core

focal species assemblage. No large-scale marine aqua-

culture takes place in the region, and we know of no

evidence that eutrophication or chemical pollution has

affected any populations of free-ranging demersal mar-

ine fish species in the Western English Channel, a region

open to Atlantic waters (Southward et al., 2005). More-

over, to our knowledge, none of the core species have

known obligate estuarine stages to their life history,

suggesting recent improvements in estuarine water

quality are unlikely to have appreciably influenced

adult population sizes of any species. Finally, neither

eutrophication or chemical pollution are known to have

contrasting influences on the abundance and size

distributions of large and small species. Most parsimo-

niously, the decline in abundance and size of the

large species of high market value is linked to over

a century of commercial fishing in the region, while

fluctuations in the abundance of small species is linked

to climate-driven regime changes in the marine

environment.

Our study system is broadly representative of other

marine fish communities within northern European

waters, containing both teleost and elasmobranch spe-

cies with a broad spectrum of life history traits and

–5

–4

–3

–2

–1

0

1

2

3

4

5

6

1910 1930 1950 1970 1990 2010

1910 1930 1950 1970 1990 2010–5–4–3–2–10123456

Year

(b)

(a)

PC

1 (m

ean

and

rang

e)P

C1

(mea

n an

d ra

nge)

Large species

Small species

Fig. 4 Temporal change in structure of the: (a) small species

and (b) large species sections of the core assemblage. Change

was captured using principal component analysis with points

closer on the PC1 axis indicating a more similar species assem-

blage. Positive increases in PC1 correspond with increases in

mean annual CPUE of the most strongly contributing species

(Table S5).

Table 3 Multiple regressions of assemblage structure (PC1) on temperature variables for subsets of large and small species

Response variable Predictor Slope SE t P

Mean annual PC1 – small species Constant �5.945 o 0.001


Summer SST focal year 0.126 0.126 0.996 0.324


Summer SST 1-year lag 0.189 0.123 1.539 0.131

Mean annual PC1 – large species Constant 2.039 0.047



Winter SST 1-year lag �0.161 0.168 �0.961 0.341

Winter SST focal year �0.0558 0.162 �0.344 0.732

Final models: small species PC1 (r2 5 0.482, F4, 43 5 9.986, Po0.001), and large species PC1 (r2 5 0.098, F4, 43 5 1.179, P 5 0.334).

PC1, principal component axis1; SST, sea surface temperature.



distributional ranges. Moreover, the region has been

subject to sustained fishing activity for over 100 years.

Thus, we suggest that our study site is representative of

many coastal habitats areas across northern Europe. It is

notable that although our study was limited in spatial

scale, similar trends have been reported in studies

undertaken over broader spatial scales, albeit over a

much shorter temporal scales. For example, analyses of

groundfish survey data from the Celtic Sea demon-

strated increases in the abundance of smaller size

classes and declines in abundance of larger individuals

between 1987 and 2003 (Blanchard et al., 2005). Equiva-

lent patterns of declines in mean trophic level of fish

caught were also detected in commercial landings data

from the same region (Pinnegar et al., 2002). Studies of

North Sea fish have found long-term declines in size

distributions (Greenstreet & Hall, 1996), and apparent

climate-related increases in the richness of smaller and

typically southern species (Hiddink & ter Hofstede,

2008). Comparisons of historic surveys with contem-

porary resurveys have also revealed declines in abun-

dance of long-lived species in the Irish Sea (Rogers &

Ellis, 2000). Taken together with our results over a

century-long scale, this evidence provides a compelling

case for widespread negative effects of fishing on size

distributions and abundance of larger species, and for

climatic influences across northern European seas.

In conclusion, we have provided evidence consistent

with contrasting effects of climate change and fishing

on different body-size components of a single marine

fish assemblage across a century-long time scale. How-

ever, reliable predictions of species responses to climate

change will require a greater understanding of popula-

tion dynamics within this system (Hart & Reynolds,

2002). This includes knowledge of behaviour in relation

to the immediate environment (Neat & Righton, 2007),

ecological interactions of species with other taxa (Beau-

grand et al., 2003), physiological tolerances (Portner &

Knust, 2007) and local evolutionary adaptations

(Hutchings et al., 2007). Our results closely match those

reported over broader spatial scales – but shorter tem-

poral scales – from other European marine fish com-

munities. As a consequence, we suggest that life history

traits are important to consider during development of

biological indicators of the effects of fishing and climate

change on marine assemblages (Rochet & Trenkel, 2003;

Blanchard et al., 2005; Greenstreet & Rogers, 2006).

Acknowledgements

We owe the availability of these data to our late co-author AlanSouthward who maintained this time series for over 40 years. Wethank captains and crew of MBA research vessels, and scientistswho contributed to these long-term data. We thank J. Partridge

and several anonymous reviewers for comments on the manu-script. This work was supported by a Great Western ResearchFellowship, the UK Department for Environment, Food andRural Affairs (Defra), and the UK Natural Environment ResearchCouncil (NERC) through Themes 6 and 10 of the Oceans 2025Strategic Research Programme, a grant-in-aid to the MBAbetween 1965 and 2007, and a NERC-Defra Sustainable MarineBioresources standard grant award NE/F001878/1.

References

Alheit J, Hagen E (1997) Long-term climate forcing of European herring

and sardine populations. Fisheries Oceanography, 6, 130–139.

Araujo JN, Mackinson S, Stanford RJ et al. (2006) Modelling food web

interactions, variation in plankton production, and fisheries in the

Western English Channel ecosystem. Marine Ecology Progress Series,

309, 175–187.

Barrett JH, Locker AM, Roberts CM (2004) The origin of intensive marine

fishing in medieval Europe: the English evidence. Proceedings of the

Royal Society of London B, 271, 2417–2421.

Beaugrand G, Brander KM, Lindley JA et al. (2003) Plankton effect on cod

recruitment in the North Sea. Nature, 426, 661–664.

Blanchard JL, Dulvy NK, Jennings S et al. (2005) Do climate and fishing

influence size-based indicators of Celtic Sea fish community structure?

ICES Journal of Marine Science, 62, 405–411.

Brander K (1981) Disappearance of common skate Raia batis from Irish

Sea. Nature, 290, 48–49.

Cook RM, Sinclair A, Stefansson G (1997) Potential collapse of North Sea

cod stocks. Nature, 385, 521–522.

Denney NH, Jennings S, Reynolds JD (2002) Life-history correlates of

maximum population growth rates in marine fishes. Proceedings of the

Royal Society of London B, 269, 2229–2237.

Dulvy NK, Polunin NVC, Mill AC et al. (2004) Size structural change in

lightly exploited coral reef fish communities: evidence for weak ecologi-

cal release. Canadian Journal of Fisheries and Aquatic Sciences, 61, 466–475.

Dulvy NK, Rogers SI, Jennings S et al. (2008) Climate change and

deepening of the North Sea fish assemblage: a biotic indicator of

warming seas. Journal of Applied Ecology, 45, 1029–1039.

Dulvy NK, Sadovy Y, Reynolds JD (2003) Extinction vulnerability in

marine populations. Fish and Fisheries, 4, 25–64.

Frank KT, Petrie B, Choi JS et al. (2005) Trophic cascades in a formerly cod

dominated ecosystem. Science, 308, 1621–1623.

Froese R (2004) Keep it simple: three indicators to deal with overfishing.

Fish and Fisheries, 5, 86–91.

Froese R, Pauly D (eds) (2008) FishBase. Available at http://www.fishbase.

org, version (10/2008) (accessed 1 January 2009).

Genner MJ, Sims DW, Wearmouth VJ et al. (2004) Regional climatic

warming drives long-term community changes of British marine fish.

Proceedings of the Royal Society of London B, 271, 655–661.

Graham NAJ, Dulvy NK, Jennings S et al. (2005) Size-spectra as indicators

of the effects of fishing on coral reef fish assemblages. Coral Reefs, 24,

118–124.

Greenstreet SPR, Hall SJ (1996) Fishing and the ground-fish assemblage

structure in the north-western North Sea: an analysis of long-term and

spatial trends. Journal of Animal Ecology, 65, 577–598.

Greenstreet SPR, Rogers SI (2006) Indicators of the health of the North Sea

fish community: identifying reference levels for an ecosystem approach

to management. ICES Journal of Marine Science, 63, 573–593.

Hart PJB, Reynolds JD (2002) Banishing ignorance: underpinning fisheries

with basic biology. In: Handbook of Fish Biology and Fisheries: Volume 1,

Fish Biology (eds Hart PJB, Reynolds JD), pp. 1–11. Blackwell Publish-

ing, Oxford.



http://www.fishbase.org



Hawkins SJ, Southward AJ, Genner MJ (2003) Detection of environmental

change: evidence from the Western English Channel. Science of the Total

Environment, 310, 245–256.

Hiddink JG, ter Hofstede R (2008) Climate induced increases in species

richness of marine fishes. Global Change Biology, 14, 453–460.

Hurst TP (2007) Causes and consequences of winter mortality in fishes.

Journal of Fish Biology, 71, 315–345.

Hutchings JA, Swain DP, Rowe S et al. (2007) Genetic variation in life-

history reaction norms in a marine fish. Proceedings of the Royal Society of

London B, 274, 1693–1699.

Jackson JBC, Kirby MX, Berger WH et al. (2001) Historical overfishing and

the recent collapse of coastal ecosystems. Science, 293, 629–638.

Jennings S, Greenstreet SPR, Reynolds JD (1999) Structural change in an

exploited fish community: a consequence of differential fishing effects

on species with contrasting life histories. Journal of Animal Ecology, 68,

617–627.

Jennings S, Kaiser MJ (1998) The effects of fishing on marine ecosystems.

Advances in Marine Biology, 34, 201–352.

Lehodey P, Alheit J, Barange M et al. (2006) Climate variability, fish, and

fisheries. Journal of Climate, 19, 5009–5030.

Levin PS, Holmes EE, Piner KR et al. (2006) Shifts in a Pacific Ocean fish

assemblage: the potential influence of exploitation. Conservation Biology,

20, 1181–90.

Mackenzie BR, Schiedek D (2007) Daily ocean monitoring since the 1860s

shows record warming of northern European seas. Global Change

Biology, 13, 1335–1347.

Myers RA, Baum JK, Shepherd TD et al. (2007) Cascading effects of the loss

of apex predatory sharks from a coastal ocean. Science, 315, 1846–1850.

Neat F, Righton D (2007) Warm water occupancy by North Sea cod.

Proceedings of the Royal Society of London B, 274, 789–798.

O’Farrell MR, Botsford LW (2006) Estimating the status of nearshore

rockfish (Sebastes spp.) populations with length frequency data. Ecolo-

gical Applications, 16, 977–986.

Perry AL, Low PJ, Ellis JR et al. (2005) Climate change and distribution

shifts in marine fishes. Science, 308, 1912–1915.

Pinnegar JK, Jennings S, O’Brien CM, Polunin NVC (2002) Long-term

changes in the trophic level of the Celtic Sea fish community and fish

market price distribution. Journal of Applied Ecology, 39, 377–390.

Portner HO, Knust R (2007) Climate change affects marine fishes through

the oxygen limitation of thermal tolerance. Science, 315, 95–97.

Revill AS, Dulvy NK, Holst R (2005) The survival of discarded lesser-

spotted dogfish (Scyliorhinus canicula) in the Western English Channel

beam trawl fishery. Fisheries Research, 71, 121–124.

Reynolds JD, Dulvy NK, Goodwin NB et al. (2005) Biology of extinction

risk in marine fishes. Proceedings of the Royal Society of London B, 272,

2337–2344.

Rochet MJ, Trenkel VM (2003) Which community indicators can measure

the impact of fishing? A review and proposals. Canadian Journal of

Fisheries and Aquatic Sciences, 60, 86–99.

Rogers SI, Ellis JR (2000) Changes in the demersal fish assemblages of

British coastal waters during the 20th century. ICES Journal of Marine

Science, 57, 866–881.

Schiermeier Q (2004) Climate findings let fishermen off the hook. Nature,

428, 4.

Sheppard C (2004) Sea surface temperature 1871–2099 in 14 cells around

the United Kingdom. Marine Pollution Bulletin, 49, 12–16.

Sims DW, Southward AJ (2006) Dwindling fish numbers already of

concern in 1883. Nature, 439, 660.

Sims DW, Wearmouth VJ, Genner MJ et al. (2004) Low-temperature-

driven early spawning migration of a temperate marine fish. Journal

of Animal Ecology, 73, 333–341.

Southward AJ, Hawkins SJ, Burrows MT (1995) Seventy years’ obser-

vations of changes in distribution and abundance of zooplankton

and intertidal organisms in the western English Channel in relation

to rising sea temperature. Journal of Thermal Biology, 20, 127–155.

Southward AJ, Langmead O, Hardman-Mountford NJ et al. (2005) Long-

term oceanographic and ecological research in the western English

Channel. Advances in Marine Biology, 47, 1–105.

Thresher RE, Koslow JA, Morison AK et al. (2007) Depth-mediated

reversal of the effects of climate change on long-term growth rates of

exploited marine fish. Proceedings of the National Academy of Sciences

USA, 104, 7461–7465.

Ward P, Myers RA (2005) Shifts in open-ocean fish communities coincid-

ing with the commencement of commercial fishing. Ecology, 86,

835–847.

Supporting Information

Additional Supporting Information may be found in the

online version of this article:

Figure S1. The spatial distribution of trawling effort between

1911 and 2007 off Plymouth, UK. Numbers in boxes indicate

the number of trawls that have taken place in the location

during the time series. The most consistently surveyed lo-

cation (378 hauls) has been the long-term sampling station L4

(Southward et al., 2005).

Table S1. Temporal distribution of demersal hauls 1911–2007.

Table S2. Composition of multi-species groups used in

analyses.

Table S3. Ship and gears dimensions of survey vessels, from

available records.

Table S4. Species length-mass relationships, samples sizes,

and predictor variables used in cross-species analyses.

Table S5. Changes in core species body size and abundance.

PCA was conducted independently on the 15 largest core

species, and the 15 smallest core species. The most extreme

loadings (o�0.4, 40.4) are underlined.

Please note: Wiley-Blackwell are not responsible for the con-

tent or functionality of any supporting materials supplied by

the authors. Any queries (other than missing material) should

be directed to the corresponding author for the article.

C L I M A T E , F I S H I N G A N D M A R I N E F I S H A S S E M B L A G E S 11


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