fishing impacts on the marine inorganic carbon cycle
TRANSCRIPT
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Fishing impacts on the marine inorganic carbon cycle
Simon Jennings1,2* and Rod W. Wilson3
1Centre for Environment, Fisheries and Aquaculture Science, Pakefield Road, Lowestoft, NR33 0HT, UK; 2School
of Environmental Sciences, University of East Anglia, Norwich, NR4 7TJ, UK; and 3School of Biosciences, Hatherly
Laboratories, University of Exeter, Exeter, Devon EX4 4PS, UK
Summary
1. Teleost fish excrete precipitated carbonate and make significant contributions to the marine inor-
ganic carbon cycle at regional and global scales. As total carbonate production is linked to fish size
and abundance, fishing is predicted to affect carbonate production by modifying fish abundance
and size-structure.
2. We draw on concepts from physiology, metabolic ecology, life history theory, population
dynamics and community ecology to develop, validate and apply analytical tools to assess fishingimpacts on carbonate production. Outputs suggest that population and community carbonate pro-
duction fall rapidly at lower rates of fishing than those used as management targets for sustainable
yield.
3. Theoretical predictions are corroborated by estimated trends in carbonate production by a
herring population and a coral reef fish community subject to fishing. Our analytical results build
on widely applicable relationships between life history parameters and metabolic rates, and can be
generalized to most fished ecosystems.
4. Synthesis and applications. If the maintenance of chemical processes as well as biological process
were adopted as a management objective for fisheries then the methods we have developed can be
applied to assess the effects of fishing on carbonate production and to advise on acceptable rates of
fishing. Maintenance of this ecosystem service would require lower rates of fishing mortality than
those recommended to achieve sustainable yield.
Key-words: community, ecosystem approach, ecosystem services, fish carbonate, fisheries,
management, population
Introduction
Fisheries managers tend to focus on achieving sustainable and
profitable fisheries while minimizing impacts on non-target
species and habitats (Sinclair & Valdimarsson 2003). However,
fisheries also impact ecosystem services and these impacts needto be assessed to determine whether they should be managed.
One important ecosystemservice provided by teleost fishis car-
bonate production, as a recent (conservative) estimate suggests
they contribute 315% of new oceanic carbonate production
globally per year and that this may account for 77262%
of carbonate dissolution in the top 1000 m of the ocean,
with implications for the acidbase balance in the upper ocean
(Wilson et al. 2009). Higher than average rates of fish carbon-
ate production and dissolution are expected in shelf seas and
upwellings, as >50% of global fish biomass occurs in these
regions (Jennings et al. 2008).
Teleost fish living in salt water precipitate carbonates in the
intestine and subsequently excrete them in mucus-coated tubes
or pellets and in the faeces (Walsh et al. 1991; Wilson et al.
1996; Wilson, Wilson, & Grosell 2002; Grosell 2006). Follow-
ing excretion, the organic parts of the tubes, pellets or faeces
rapidly degrade, leaving inorganic crystals of calcium carbon-ate (Walsh et al. 1991). Carbonate precipitates are formed
whether or not the fish are feeding (Wilson et al. 1996; Taylor
& Grosell 2006) because the essential process of drinking
seawater results in the supersaturation of calcium and magne-
sium carbonates in the intestine (Wilson et al. 2002; Wilson &
Grosell 2003). Walsh et al. (1991) suggested that carbonate
excretion might make a significant contribution to the
inorganic carbon cycle, and this has since been confirmed by
the global analysis of Wilson et al. (2009). Fish carbonates
have a higher magnesium content and are therefore expected
to have greater solubility than other marine carbonates. This
would result in faster dissolution with depth, providing a novel
explanation for much of the increase in titratable alkalinity
within upper 1000 m of the ocean (Wilson et al. 2009).*Correspondence author. E-mail: [email protected]
Journal of Applied Ecology 2009, 46, 976982 doi: 10.1111/j.1365-2664.2009.01682.x
2009 The Authors. Journal compilation 2009 British Ecological Society
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The rate of carbonate production by fish is assumed to be
proportional to the seawater drinking rate and metabolic rate
(Takei & Tsukada 2001). This is because osmoregulatory pro-
cesses such as drinking and active ion transport serve to coun-
terbalance passive ion and water fluxes (primarily at the gills)
and these passive fluxes (water loss and ion gain in marine fish,and the opposite in freshwater fish) are directly proportional to
gill ventilation and perfusion and therefore proportional to the
oxygen uptake rate and metabolic rate (Nilsson 1986; Gonz-
alez & McDonald 1992). As the metabolic rates of individuals
and species vary with environmental temperature and body
size (Clarke & Johnston 1999; Glazier 2005), the temperature
of the surrounding environment as well as the size composition
and total abundance of a fish population or community, will
determine the total rate of carbonate production.
Fishing takes place in all the global oceans and has substan-
tially modified the structure of fish populations and communi-
ties. Of those factors that influence rates of carbonate
production by fish communities, both total biomass and size
structure are affected by fishing (Quinn & Deriso 1999; Bianchi
et al. 2000; Shin et al. 2005). Comparisons among areas subject
to different fishing intensities and temporal comparison within
areas where fishing effort has increased over time, have both
shown that increased fishing mortality is associated with
decreases in total biomass and a shift in the size distribution
from larger to smaller individuals (Bianchi et al. 2000; Shin
et al. 2005).
Here, we develop, validate and apply methods for describing
relationships between fishing intensity and carbonate produc-
tion by fish populations and communities. These methods can
be used to predict how the size composition and abundance offish communities changes in response to fishing mortality and
the consequent impact on rates of carbonate production. Our
new methods provide a quantitative approach for assessing
whether the management of renewable resources should focus
on chemistry as well as biology, an important step in incorpo-
rating concerns about the sustainability of ecosystem services
into environmental management.
Materials and Methods
The analyses comprise fourstages: (i) development of a model linking
fish carbonate production to body mass and temperature, (ii) devel-
opment of a model of fishing effects on population carbonate produc-
tion, (iii) development of a model of fishing effects on community
carbonate production, and (iv) validation and application of the
models, based on data that demonstrate fishing-related changes in
the body size composition and abundance of a population and
community.
C A R B O N A T E P R O D U C T I O N
A model that links the rate of carbonate production to fish body size
and temperature was used to estimate rates of carbonate production.
This is based on the observation that rates of drinking by fish are
directly proportional to metabolic rate, and that drinking rates deter-
mine rates of carbonate production (Takei & Tsukada 2001; Wilsonet al. 2002; Taylor & Grosell 2006). Given this indirect link between
carbonate production and metabolic rate, changes in relative rates of
carbonate production with temperature can be approximated with
the Arrhenius relationship. This relationshipprovidesa good descrip-
tion, but not a causal explanation, of the effects of temperature on
metabolic rate(e.g. Clarke& Johnston 1999). TheArrhenius relation-
ship
R AeE=kT eqn 1
links the rate coefficients of a chemical reaction (R) to the absolute
temperature T, where A is a prefactor, E is the activation energy of
the reaction and k is the Boltzmann constant (or the Gas constant
when E is expressed in molar units). Over biologically relevant tem-
perature ranges E is assumed to be independent of temperature and
the minor temperature dependenceofA is regarded as negligiblecom-
pared with the temperature dependence of the e)E kTterm (Clarke &
Johnston 1999).
Takingthe natural logsof the Arrhenius equation gives:
loge R Ek1T loge A eqn 2
thusa plotof logeR vs T)1 is a straightline of slope Ek and intercept
logeA. This approach was used to estimate )Ek from the data com-
pilation of Clarke & Johnston (1999) that listed temperature and pre-
dicted resting (standard) metabolic rates for a range of fish species at
body mass 50 g. Therelationship washighly significant F = 81451,88
(P < 00001), slope ()Ek) was )472736 (95% C.I. )36864 to
)57683) and theintercept was 1427(95%C.I. 10591795).
We assumed that the scaling of metabolism with body mass (W),
both within and among species, could be approximated as W075. In
reality, the value of the exponent can vary within and among species
(Clarke& Johnston 1999; Glazier 2005) but we consider W075 an ade-
quate approximation for developing a generically applicable
approach, and the exponent could easily be modified in the subse-
quent equations if species-specific data were available. We combined
the relationship between body mass and metabolism with the Arrhe-
nius equation describing temperature effects following the approach
of Gillooly et al. (2002). Assuming that the rate of metabolism is pro-
portional to the rate of carbonate production C (given the effects of
metabolism on drinking rate; Takei & Tsukada 2001)
C aqaW0:75AeE=kT eqn 3
where a is a constant. Constantsa andqwere added to correct experi-
mentally measured mass specific rates of carbonate production (Wil-
son et al. 2009) for the ratio between carbonate production in activeand resting fish (a) and the relatively higher resting metabolism and
drinking rates of fish species living in the water column (q) (Clarke &
Johnston 1999; Takei & Tsukada 2001). Alpha exceeds one in wild
fish because metabolic rate, and hence drinking rate and carbonate
production, rise above resting (experimental) levels during normal
activity (Kerr 1982). Carbonate production per unit mass can thus be
expressed as
C=W aqaW0:25AeE=kT eqn 4
To fit equation (4) to data for resting unfed benthic fish, the values of
a and q were both set to one. This equation was fitted to data for car-
bonate production per unit mass by Gulf toadfish Opsanus beta andEuropean flounder Platichthys flesus, as recorded experimentally in
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resting unfed fish (Walsh et al. 1991; Wilson et al. 2002; Taylor &
Grosell 2006; Taylor et al. 2007), to determine constants a and A, giv-
ing the equation
C=W aq9:81 108W0:25e47271=T eqn 5
where carbonate production per unit mass is expressed as l mol C
kg)1 h)1 (molarC = g C12), Wis bodymass in g and Tis tempera-
ture in Kelvin (C+273) (Wilson et al. 2009). We set the valueofa to
25 to q 24 based on the differences between resting and activity
metabolism and the relative activity levels of bottom living and pela-
gic fishes reported in Wilson et al. (2009). For simplicity, and given
the very limited data currently available to parameterise the model,
we assume the same model applies within and among species. How-
ever, the general formof the model willallow it to be re-parameterised
if additional data on rates of carbonate productionare collected.
F I S H I N G E F F E C T S O N P O P U L A T I O N S
Total carbonate production by a population at a given temperaturedepends on size composition and abundance. Changes in carbonate
production by a cohort (year class) with time are a function of the
changes in the number of individuals owing to mortality and the
changes in the size of individuals owing to growth. The number of
individuals in a cohort at time t can be estimated using (e.g. Quinn &
Deriso 1999)
Nt N0eMFt eqn 6
where N0 is the number of individuals present at t = 0, F is fishing
mortality and M is natural mortality. The von Bertalanffy Growth
Equation can be used to describe W at time t as a function of the
asymptotic mass W(e.g. Quinn & Deriso 1999)
Wt W11 eKtt0 3 eqn 7
where t0 is the time when W is theoretically zero and K is the Brody
growthcoefficient.
Following equation 3, carbonateproduction at time t will be
Ct NtaqaW0:75t Ae
E=kT eqn 8
where Nt is the number of individuals present at time t as determined
from equation (6) and Wt is determined from equation (7). Assuming
temperature is constant through the cohort lifespan, the time when a
cohort is producing the maximum amount of carbonate tCmax can
thus be determined by substituting (6) and (7) into (8), differentiatingwithrespect to t andsolving for tCmax whenthe first derivative is set to
zero.
tCmax t0 loge 1 9
4
K
M F
1=Keqn 9
Equation (9) can be substituted into (7) to give the weight of fish in a
cohort when they are producing the maximum amount of carbonate
WCmax andthe equation for WCmax reduces to
WCmax W1 1= 1M F
2:25K
3eqn 10
The advantage of equations (9) and (10) is that for F = 0, the
MKratio, which is relatively constant among many fish populations
(Beverton 1992), can be used to predict the time and body mass when
an unexploited cohort is producing most carbonate. This allows the
application of the method when Mand Karenot known separately.
Observed values of tCmax and WCmax in fished populations can be
compared with theoretical values for unfished populations, providing
an indicator of the relative impacts of fishing on carbonate produc-
tion.
As most fish populationassessments areage based, a summation of
Ct across age classes up to the maximum age tmax provides an ade-
quate assessment of total carbonate production throughout the life-
span of a cohort Ctotp (and hence the carbonate production of a
populationat steady state). This is given by
Ctotp Xtmaxt0
F MtNtaqaW075t Ae
E=kT eqn 11
The methods of population-based analysis were applied to the her-
ring population in the North Sea, for which there are long-term age-
structured data and very large fluctuations in abundance and mortal-
ity over time (ICES 2007). We estimated carbonate production based
on a full age-structured population assessment for the fished popula-
tion and for the population in the absence of fishing. The life history
parameters of the herring population were W = 332g, t0 = )11,
K = 04 and mean M = 031, with age-specific M based on ICES
(2007) in the age-structured analysis. Mean sea temperature in the
North Sea was taken as 105 C (ICES, unpublished data).
F I S H I N G E F F E C T S O N C O M M U N I T I E S
To assess the potential effects of fishing on carbonate production by
fish communities we modified a model that captures the direct and
indirect effects of fishing on community abundance and size structure
(Pope et al. 2006). The model predicts interrelationshipsbetween fish-
ing, population and community dynamics that are supported by
empirical analysis and uses 15 parameters to describe a 13 speciesfish community, where species are defined by their maximum body
size (asymptotic length L) and size-related life history parameters.
An overall Facts on all species and can be modified by defining spe-
cies and size selectivity. The parameter values followed the key run
of Pope et al. (2006) but the exploitation pattern was modified so that
all species were fished at the same F. This pattern is indicative of
exploitation in many multispecies fisheries where small and large
fishes are targeted. The model is intended to mimic the effects of fish-
ing in a shallow (typically
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of areas subject to different levels of fishing effort thatincluded lightly
or unfished areas (Jennings & Polunin 1997).
Fish abundance was determined by underwater visual censusin ten
reef fishing grounds on the western coast of Kadavu Island, Fiji. The
boundaries of each fishing ground enclose areas of reef where people
from specific villages have exclusive rights to fish. As a result, varia-
tions in human population density and reef area among grounds
mean that they are subject to a range of fishing intensities. Reef fishes
in the families studied do not move extensively among grounds and
thus their abundance is determined by the recruitment of larvae from
the plankton, natural mortality and local fishing intensity. Further
details of the study areas, associatedfish communities, datacollection
andprocessingare provided in Jennings & Polunin (1997).
All fish census work was conducted in 1995 and 1996 and 144 spe-
cies were censused. Abundances were determined at seven randomly
selected replicate sites in each of the fishing grounds. At each site, the
abundance and size of census species 8 cm length was estimated
within 12 adjacent census areas of 7 m radius by counting each fish
and estimating its length to 1 cm. Species in each census area were
recorded sequentially, with the most active species being first. Whena count for one species was complete, all further movements of that
species were disregarded. Fish lengths were converted to mass from
published lengthmass relationships. Carbonate production was cal-
culated from mass at a temperature of 275 C, the annual mean
water temperature (NOAA 2007).
An index of fishing intensity in each fishing ground was calculated
by dividing the number of people in the villages that have fishing
rights in the fishing grounds by the length of reef front. In Fijian vil-
lages, all villagers have fishing rights and so the population approxi-
mates the number of fishers and consumers (Jennings & Polunin
1997). Human population data were obtained from the most recent
census. The length of reef front was measured on aerial photographs
or navigational charts.
Results
The theoretical analysis of relationships between the body
weight at which a cohort has maximum carbonate production
WCmax, asymptotic weight W and fishing mortality F
showed that WCmax was 216% ofW in the absence of fish-
ing and decreased to 60% from the value when
F = 0. Total carbonate production by the population (Ctotp)
as a proportion ofCtotp when F = 0 is almost linearly related
to WCmaxW (Fig. 1c).
Estimated carbonate production per recruit by the North
Sea herring population fluctuated from 1960 to 1996 (Fig. 2a)
and, when CR was expressed as a proportion of CRF = 0, it
was negatively correlated with fishing mortality (Fig. 2b).
Total carbonate production varied substantially among
cohorts and among years, with both trends tending to precede
decreases in total population biomass (Fig. 3).
The relationship between the age at maximum carbonate
production tCmax or WCmax and Ffor herring (Fig. 4) showedthat tCmax or WCmax would be expected to occur early in life
and at low body mass if the population were fished at
F = 068; the mean F in the period 19601996. At the target
F of 025 (ages 26) which applies when spawning population
biomass is >13 106 tonnes (ICES 2007), carbonate produc-
tion at tCmax or WCmax would be more than double the value at
F = 068. The predicted tCmax or WCmax for the population
are broadly consistent with the values calculated from the age-
structured assessment, with the age 0 group always having
highest estimated carbonate production from 1960 to 1996 and
average mass of this group being 13 g.
The model of the effects of fishing on carbonate production
suggested that the greatest decreases in community carbonateproduction would occur at relatively low rates of mortality
Fishing mortality
Rela
tiveC/RorY/R
00
02
04
06
08
10
(a)
(b)
(c)
00 02 04 06 08 10
Fishing mortality
00 02 04 06 08 10
WCmax
/W
WCmax/W
000
005
010
015
020
025
005 010 015 020 025
Re
lativeCtotp
00
02
04
06
08
10
Fig. 1. Relationships between (a) body mass at maximum carbonate
production as a proportion of asymptotic mass (WCmaxW) and
fishing mortality, (b) relative carbonate production per recruit (con-
tinuous line) or yield per recruit (solid line) and fishing mortality and
(c) relative carbonate production by the population (CtotpCtotpF=0)
and body mass at maximumcarbonate production as a proportion of
asymptotic mass (WCmaxW). We assumed W = 1000, k = 03
and MK = 15.
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(Fig. 5a). At F = 05, relative carbonate production had fallen
to about 60% of that in the unfished community. At higher
rates of F, there was relatively little change in the rate of car-bonate production. The rate of decrease in carbonate produc-
tion with fishing was slightly lower than the rate of decrease in
total biomass (Fig. 5a). The mean mass of individuals in the
modelled community broadly declined with increasing fishing
mortality while the mean rate of carbonate production per unit
mass showed a corresponding increase (Fig. 5b). In these simu-
lations, F = 025 corresponded to the multispecies Fat which
the maximum sustainable yield could be taken from the most
vulnerable species, while maximum multispecies yield would
be taken at F > 10.
Fishing intensity in the Fijian reef fisheries was expressed in
terms of effort rather than F, owing to the absence of data
describing population-specific exploitation rates. The range of
fishing effort spanned more than an order of magnitude with
one ground infrequently fished. Community biomassdecreased rapidly with low and increasing levels of fishing
effort but stabilized at higher effort (Fig. 6a). Estimated car-
bonate production was highest in the least frequently fished
ground, on average 20% higher than at other grounds, where
production was lower and more variable, and did not show a
clear relationship with fishing intensity (Fig. 6b). Carbonate
production per unit biomass increased with fishing effort,
probably reflecting the dominance of smaller fishes that pro-
duce more carbonate per unit mass in the more heavily
exploited grounds (Fig. 6c).
Discussion
For populations and communities, lower rates of fishing mor-
tality than those associated with obtaining high and sustain-
able yields lead to substantial reductions in population
carbonate production. Relatively small changes in rates of
carbonate production at higher fishing mortalities imply that
current management interventions intended to achieve high
and sustainable yield will have limited effects on carbonate
production. The analytical methods and hence the results
depend on widely applicable relationships between mortality,
population and community size structure and metabolism, and
we therefore expect they can be generalized to populations and
communities in most fished ecosystems. In general, fishingmortality reduces total carbonate production and CR in the
Fishing mortality F
00 02 04 06 08 10 12 14 16 18
C/Ra
sproportionC
/RF=
0
015
020
025
030
035
Year class
1960 1970 1980 1990
C/R(
g)
06
07
08
09
10
11(a)
(b)
Fig.2. Predicted carbonate production per recruit for the North Sea
herring stock for the year classes from 1960 to 1996 (a) and the rela-
tionship between CR as a proportion CRF = 0 and thefishing mor-tality (Fforages 36) in each of thesecohorts (b).
Year class or year
1960 1970 1980 1990
CaCO3(103t
onnesyears1)
0
20
40
60
80
100
120 Populationbiomass(106tonnes)
0
1
2
3
4
5
CaCO3 by cohortsCaCO3 by yearspopulation biomass
Fig.3. Trends in estimated CaCO3 production by the North Sea
herring population by cohorts (closed circles, solid line) and by years
(open circles, broken line) from 1960 to 1996 Total population
biomass over the same time period is shown with the dotted line and
small circles.
WCm
ax t
Cmax
00
05
10
15
20
25
Fishing mortality F
00 02 04 06 08 100
50
100
150
200
Fig.4. Relationship between WCmax (solid line) and tCmax (broken
line) andfishingmortalityfor the North Sea herring population.
980 S. Jennings & R. W. Wilson
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population because the abundance of fished cohorts will fall
more rapidly with age. However, carbonate production per
unit mass increases with fishing mortality in fished populations
and communities because these are dominated by smaller indi-viduals.
The model that links size and temperature to carbonate
production assumed that the intercepts of relationships
between R and C and W were the same for all species. This
would not be the case in reality, as active species of pelagic fish
(e.g.tunas) have higher metabolic rates than less active bottom-
dwelling species (e.g. groupers, flatfishes) at a given body size
and temperature (Clarke & Johnston 1999) and this would
influence their drinking rates. However, the model structure is
sufficiently general that it could easily be parameterised with
species-specific data as they become available. In the case of
the community analysis, larger bottom-dwelling species do
tend to be more vulnerable to fishing than smaller pelagic
species and changes in their relative abundance could lead to
relative increases in the rate of carbonate production per unit
biomass at different fishing intensities. The predicted trend in
carbonate production with fishing will also be influenced by
the proportion of teleosts (carbonate producing) and elasmo-
branchs (not carbonate producing) in the fish community.
Elasmobranchs tend to have relatively large body sizes and to
be more vulnerable to fishing owing to their low intrinsic rates
of increase (Stevens et al. 2000), so it might be expected that
they will form a smaller proportion of total biomass at high
fishing mortality. This would exaggerate any predicted
decrease in carbonate production.
The relationship between WCmax and W provides a linearindicator of the extent to which relative carbonate production
Fishing effort (persons km2 reef front)
0 50 100 150 200 250 300010
012
014
016
018
020
45
50
55
60
65
70
75
80
85
Biomass(
gm
2)
C
pro
duc
tion
(g
m
2y
ears
1)
C
pro
duc
tionperuni
tbiomass
(gg
1)
20
30
40
50
60
70
80(a)
(c)
(b)
Fig. 6. Relationships between (a) biomass, (b) carbonate production
and (c) carbonate production per unit mass and fishing effort on
Fijian reef fishing grounds. Vertical bars are 95% confidence inter-
vals.
00
02
04
06
08
10
Carbona
tepro
duc
tion
(C)as
proport
ion
CF=
0
Biomass(B)asproportionBF=0
00
02
04
06
08
10
(a)
(b)
Fishing mortality F
00 02 04 06 08 10 12 14
00 02 04 06 08 10 12 14
Mean
individua
lmass
(g)
26
28
30
32
34
36
38
4042
44
08
09
10
11
12
13
C
orbonateproductionperunit
biomass(relative)
Fig. 5. (a) Changes in total carbonate production (continuous line)
and relative biomass (broken line) of a fish community as a function
of changes in the rate of fishing mortality The rate of carbonate pro-
duction (Ctotc) and biomass (B) are expressed as a proportion of their
values with no fishing (F = 0). (b) Relationship between mean indi-
vidual body mass (continuous line) or carbonate production per unit
biomass (broken line) and fishing mortality in the modelled fish com-
munity.
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per recruit and total carbonate production of a population at
steady state is influenced by fishing. WCmax can be calculated
without a natural mortality for the species concerned, by tak-
ing advantage of the MK ratio, and thus provides a simple
method for assessing the relative effects of fishing on carbonate
production. The disadvantage of this simple technique overage-structured assessment ofCR is the assumption of a single
value ofMin all age classes, when fish typically exhibit higher
Mwhen younger. If size or age-related natural mortality data
are available for some well-studied populations, our analyses
show that it would be straightforward to modify existing popu-
lation assessment methods to predict the effect of various rates
of fishing mortality on Ctotp and CR.
This analysis suggests that fishing will alter the rates of car-
bonate production by fish populations and communities, but
the analysis would be refined by significant additional research,
to include (i) obtaining carbonate production data for a wider
range of species, body sizes and temperatures to better para-
meterise the model linking these variables, (ii) accounting for
differences in the relative activity levels of fishes in the carbon-
ate production modeland in the predictions of changes in com-
munity structure, (iii) accounting for the effects of fishing on
carbonate production by the smaller size-classes of fish, and
(iv) accounting for changes in relative abundance of teleosts
and elasmobranchs in the model of fishing impacts. In addi-
tion, while the analyses provide a method for giving manage-
ment advice on the effects of fishing on an ecosystem service
other than food production, considerable work would still be
needed to identify realistic management objectives for this
service. Such objectives would ultimately be a matter of choice
for society, albeit informed by science (Jennings 2007). Ourunderstanding of the wider consequences of changes in the
rates of fish carbonate production on ocean chemistry and the
consequences for biota will need to be improved to inform any
debate on objectives.
Acknowledgements
We thank Andrew Clarke for providing the compilation of teleost oxygen con-
sumption data from Clarke & Johnston (1999) and John Pope for allowing us
to modifythe size-based model of Pope etal. (2006)for thisanalysis.S.J. thanks
UK DFID (formerly ODA) and NERC for funding the collection of the fish
community data used in this analysis, and the EC and Defra for funding this
research. R.W.thanks BBSRC andThe Royal Societyfor fundingfundamental
studieson intestinalcarbonateproduction in marine fish.
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Received7 March2009;accepted 9 June 2009
Handling Editor: NickDulvy
982 S. Jennings & R. W. Wilson
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Applied Ecology, 46, 976982