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Keywords:

  • community;
  • ecosystem approach;
  • ecosystem services;
  • fish carbonate;
  • fisheries;
  • management;
  • population

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

1.  Teleost fish excrete precipitated carbonate and make significant contributions to the marine inorganic 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 fishing impacts on carbonate production. Outputs suggest that population and community carbonate production 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.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

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 need to be assessed to determine whether they should be managed. One important ecosystem service provided by teleost fish is carbonate production, as a recent (conservative) estimate suggests they contribute 3–15% of new oceanic carbonate production globally per year and that this may account for 7·7–26·2% of carbonate dissolution in the top 1000 m of the ocean, with implications for the acid–base balance in the upper ocean (Wilson et al. 2009). Higher than average rates of fish carbonate 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). Following excretion, the organic parts of the tubes, pellets or faeces rapidly degrade, leaving inorganic crystals of calcium carbonate (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 magnesium 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).

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 processes such as drinking and active ion transport serve to counterbalance 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; Gonzalez & 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 substantially modified the structure of fish populations and communities. 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 production by fish populations and communities. These methods can be used to predict how the size composition and abundance of fish 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 incorporating concerns about the sustainability of ecosystem services into environmental management.

Materials and Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The analyses comprise four stages: (i) development of a model linking fish carbonate production to body mass and temperature, (ii) development of a model of fishing effects on population carbonate production, (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.

Carbonate Production

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 determine rates of carbonate production (Takei & Tsukada 2001; Wilson et 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 relationship provides a good description, but not a causal explanation, of the effects of temperature on metabolic rate (e.g. Clarke & Johnston 1999). The Arrhenius relationship

  • image( 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 temperature ranges E is assumed to be independent of temperature and the minor temperature dependence of A is regarded as negligible compared with the temperature dependence of the eE/kTterm (Clarke & Johnston 1999).

Taking the natural logs of the Arrhenius equation gives:

  • image( eqn 2)

thus a plot of logeR vs T−1 is a straight line of slope –E/k and intercept logeA. This approach was used to estimate −E/k from the data compilation of Clarke & Johnston (1999) that listed temperature and predicted resting (standard) metabolic rates for a range of fish species at body mass 50 g. The relationship was highly significant F = 81·451,88 (< 0·0001), slope (−E/k) was −4727·36 (95% C.I. −3686·4 to −5768·3) and the intercept was 14·27 (95% C.I. 10·59–17·95).

We assumed that the scaling of metabolism with body mass (W), both within and among species, could be approximated as W0·75. In reality, the value of the exponent can vary within and among species (Clarke & Johnston 1999; Glazier 2005) but we consider W0·75 an adequate approximation for developing a generically applicable approach, and the exponent could easily be modified in the subsequent equations if species-specific data were available. We combined the relationship between body mass and metabolism with the Arrhenius equation describing temperature effects following the approach of Gillooly et al. (2002). Assuming that the rate of metabolism is proportional to the rate of carbonate production C (given the effects of metabolism on drinking rate; Takei & Tsukada 2001)

  • image( eqn 3)

where a is a constant. Constants α and ρ were added to correct experimentally measured mass specific rates of carbonate production (Wilson et al. 2009) for the ratio between carbonate production in active and resting fish (α) and the relatively higher resting metabolism and drinking rates of fish species living in the water column (ρ) (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

  • image( eqn 4)

To fit equation (4) to data for resting unfed benthic fish, the values of α and ρ were both set to one. This equation was fitted to data for carbonate production per unit mass by Gulf toadfish Opsanus beta and European flounder Platichthys flesus, as recorded experimentally in resting unfed fish (Walsh et al. 1991; Wilson et al. 2002; Taylor & Grosell 2006; Taylor et al. 2007), to determine constants a and A, giving the equation

  • image( eqn 5)

where carbonate production per unit mass is expressed as μ mol C kg−1 h−1 (molar C = g C/12), W is body mass in g and T is temperature in Kelvin (°C+273) (Wilson et al. 2009). We set the value of α to 2·5 to ρ 2·4 based on the differences between resting and activity metabolism and the relative activity levels of bottom living and pelagic 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. However, the general form of the model will allow it to be re-parameterised if additional data on rates of carbonate production are collected.

Fishing Effects on Populations

Total carbonate production by a population at a given temperature depends 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)

  • image( 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)

  • image( eqn 7)

where t0 is the time when W is theoretically zero and K is the Brody growth coefficient.

Following equation 3, carbonate production at time t will be

  • image( 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), differentiating with respect to t and solving for tCmax when the first derivative is set to zero.

  • image( eqn 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 and the equation for WCmax reduces to

  • image( eqn 10)

The advantage of equations (9) and (10) is that for F = 0, the M/K ratio, 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 M and K are not 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 production.

As most fish population assessments are age based, a summation of Ct across age classes up to the maximum age tmax provides an adequate assessment of total carbonate production throughout the lifespan of a cohort Ctotp (and hence the carbonate production of a population at steady state). This is given by

  • image( eqn 11)

The methods of population-based analysis were applied to the herring population in the North Sea, for which there are long-term age-structured data and very large fluctuations in abundance and mortality over time (ICES 2007). We estimated carbonate production based on a full age-structured population assessment for the fished population and for the population in the absence of fishing. The life history parameters of the herring population were W = 332g, t0 = −1·1, K = 0·4 and mean M = 0·31, with age-specific M based on ICES (2007) in the age-structured analysis. Mean sea temperature in the North Sea was taken as 10·5 °C (ICES, unpublished data).

Fishing Effects on Communities

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 interrelationships between fishing, population and community dynamics that are supported by empirical analysis and uses 15 parameters to describe a 13 ‘species’ fish community, where species are defined by their maximum body size (asymptotic length L) and size-related life history parameters. An overall F acts on all species and can be modified by defining species 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 fishing in a shallow (typically <200 m depth) shelf sea ecosystem, and was extended to output relative carbonate production.

As the W and length (L) in fish are typically related as W ∝ L3, the scaling of C/W and L will be ∝ L−0·75 if the scaling of C/W and W is ∝ W−0.25. The total relative carbonate production of the fish community (Ctotc) at different levels of fishing mortality F was thus defined as

  • image( eqn 12)

where Lmin and Lmax were taken as 5 cm and 130 cm and values of weight at length (WL) and numbers at length (NL) for 10 cm size classes were output from the model.

The theoretical analysis of fishing effects on carbonate production suggested that the largest changes in carbonate production would occur at relatively low levels of fishing mortality. Therefore, to corroborate or reject this pattern we needed to analyse empirical data from areas with very low levels of fishing mortality. Most fisheries time series data were collected well after exploitation rates exceeded = 0·3 or 0·4 and thus we analysed data from spatial comparisons of areas subject to different levels of fishing effort that included lightly or unfished areas (Jennings & Polunin 1997).

Fish abundance was determined by underwater visual census in 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, variations 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, associated fish communities, data collection and processing are provided in Jennings & Polunin (1997).

All fish census work was conducted in 1995 and 1996 and 144 species 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. When a count for one species was complete, all further movements of that species were disregarded. Fish lengths were converted to mass from published length–mass relationships. Carbonate production was calculated from mass at a temperature of 27·5 °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 villages, all villagers have fishing rights and so the population approximates 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

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

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 21·6% of W in the absence of fishing and decreased to <5% of W as F increased to 1·0 (Fig. 1a). Carbonate production per recruit (C/R) decreased by 90% over this range of fishing mortality, with a faster rate of decrease per unit increase in F at lower F (Fig. 1b). Indeed, when yield per recruit (Y/R) attains the maximum value (F≈0·3), C/R has decreased by >60% from the value when = 0. Total carbonate production by the population (Ctotp) as a proportion of Ctotp when = 0 is almost linearly related to WCmax/W (Fig. 1c).

image

Figure 1.  Relationships between (a) body mass at maximum carbonate production as a proportion of asymptotic mass (WCmax/W) and fishing mortality, (b) relative carbonate production per recruit (continuous line) or yield per recruit (solid line) and fishing mortality and (c) relative carbonate production by the population (Ctotp/CtotpF=0) and body mass at maximum carbonate production as a proportion of asymptotic mass (WCmax/W). We assumed W = 1000, = 0·3 and M/= 1·5.

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Estimated carbonate production per recruit by the North Sea herring population fluctuated from 1960 to 1996 (Fig. 2a) and, when C/R was expressed as a proportion of C/R= 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).

image

Figure 2.  Predicted carbonate production per recruit for the North Sea herring stock for the year classes from 1960 to 1996 (a) and the relationship between C/R as a proportion C/R= 0 and the fishing mortality (F for ages 3–6) in each of these cohorts (b).

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image

Figure 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.

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The relationship between the age at maximum carbonate production tCmax or WCmax and F for herring (Fig. 4) showed that tCmax or WCmax would be expected to occur early in life and at low body mass if the population were fished at = 0·68; the mean F in the period 1960–1996. At the target F of 0·25 (ages 2–6) which applies when spawning population biomass is >1·3 × 106 tonnes (ICES 2007), carbonate production at tCmax or WCmax would be more than double the value at = 0·68. 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.

image

Figure 4.  Relationship between WCmax (solid line) and tCmax (broken line) and fishing mortality for the North Sea herring population.

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The model of the effects of fishing on carbonate production suggested that the greatest decreases in community carbonate production would occur at relatively low rates of mortality (Fig. 5a). At = 0·5, 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 carbonate production. The rate of decrease in carbonate production 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 simulations, F = 0·25 corresponded to the multispecies F at which the maximum sustainable yield could be taken from the most vulnerable species, while maximum multispecies yield would be taken at > 1·0.

image

Figure 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 production (Ctotc) and biomass (B) are expressed as a proportion of their values with no fishing (= 0). (b) Relationship between mean individual body mass (continuous line) or carbonate production per unit biomass (broken line) and fishing mortality in the modelled fish community.

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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 biomass decreased rapidly with low and increasing levels of fishing effort but stabilized at higher effort (Fig. 6a). Estimated carbonate 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 produce more carbonate per unit mass in the more heavily exploited grounds (Fig. 6c).

image

Figure 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 intervals.

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

For populations and communities, lower rates of fishing mortality than those associated with obtaining high and sustainable 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, fishing mortality reduces total carbonate production and C/R in the 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 individuals.

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 elasmobranchs (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 linear indicator of the extent to which relative carbonate production 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 taking advantage of the M/K ratio, and thus provides a simple method for assessing the relative effects of fishing on carbonate production. The disadvantage of this simple technique over age-structured assessment of C/R is the assumption of a single value of M in all age classes, when fish typically exhibit higher M when 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 population assessment methods to predict the effect of various rates of fishing mortality on Ctotp and C/R.

This analysis suggests that fishing will alter the rates of carbonate 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 parameterise the model linking these variables, (ii) accounting for differences in the relative activity levels of fishes in the carbonate production model and in the predictions of changes in community 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 addition, while the analyses provide a method for giving management 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). Our understanding 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

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We thank Andrew Clarke for providing the compilation of teleost oxygen consumption data from Clarke & Johnston (1999) and John Pope for allowing us to modify the size-based model of Pope et al. (2006) for this analysis. 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 and The Royal Society for funding fundamental studies on intestinal carbonate production in marine fish.

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  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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