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The evolutionary pressure from shing on size at maturation of Baltic cod

K.H. Andersen a, , K.D. Farnsworth b , U.H. Thygesen a , J.E. Beyer a
a b

Danish Institute for Fisheries Research, Technical University of Denmark, Charlottenlund Castle, DK-2920 Charlottenlund, Denmark School of Biological Science, Queens University Belfast, 97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, UK

a r t i c l e
Article history:

i n f o

a b s t r a c t
Recent observations suggest shing pressure is driving the evolution of smaller female maturation size in some sh stocks. We construct a general size-based theoretical framework to derive the rate and ultimate destination of this evolution based on life-history, community ecology and evolutionary theory. For Baltic cod (Gadus morhua), we nd a maximum evolutionary rate of approximately 36 g/generation (0.072 Haldanes) and optimum maturation size < 250 g (mean 50 g). Whilst this is consistent with many previous observations, it is substantially less than observed in rapidly declining cod stocks, suggesting additional evolutionary processes may affect them. Analysis of management remedies nds only an effective ban on shing will halt the evolution. Unable to maximise tness, the sh will remain under evolutionary stress for the foreseeable future. 2007 Elsevier B.V. All rights reserved.

Received 21 April 2006 Received in revised form 2 January 2007 Accepted 4 January 2007 Published on line 9 February 2007 Keywords: Fisheries-induced evolution Life-history evolution Baltic cod Age at maturation Harvest Gadus morhua

1.

Introduction

Recent observations show a decline of maturation size in some heavily exploited cod stocks, with evidence pointing to evolution induced by size-selective shing as the cause (Olsen et al., 2004; Barot et al., 2004). This hypothesis is corroborated by both experimental studies (Reznick and Ghalambor, 2005) and empirical evidence from other sheries (Grift et al., 2003). However the theoretical developments needed to predict the rate and destination of this evolution and its likely consequences in general for sheries have been limited to the special case developed for the north-east Arctic cod population, which has had an unusual exploitation pattern (Law and Grey, 1989; Jrgensen and Fiksen, 2006).

The concept of sheries-induced evolution and its effects on the yield of an exploited sh stock was pioneered by Law and Grey (1989), with a theoretical work on north-east Arctic cod. They showed how shing pressure creates a strong selection for individuals with early maturation, leading to a change in the age at maturation of the stock, towards earlier maturation. Recently interest in the topic has been increasing, and statistical methods has been developed, demonstrating that changes in maturity ogives for north-west Atlantic cod stocks are likely due to changes in the distribution of genotypes in the stock, and not only due to phenotypic plasticity (Barot et al., 2004; Olsen et al., 2004). The most modelled stock is the north-east Atlantic cod stock (Law and Grey, 1989; Heino, 1998; Jrgensen and Fiksen, 2006). This stock is however special, as

Corresponding author. E-mail address: kha@difres.dk (K.H. Andersen). 0304-3800/$ see front matter 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.ecolmodel.2007.01.002

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it traditionally before modern trawlers has had an exploitation pattern where shing was largely conned to the mature part of the population. This has been going on for centuries, and resulted in an evolutionary pressure for late maturation, as it was protable to post-pone maturation, and thus delay the risk of shing mortality. When shing commenced on the immature part of the population, that pressure was reversed, and a trend of declining age at maturation was initiated (Law and Grey, 1989). One reason for the interest in sheries-induced evolution has been to use a rapid decline in age at maturation as an indicator of unsustainable exploitation of a stock. Another has been to explicitly take the evolution into account in the management of the stock (Heino, 1998). A recent interesting conjecture by Conover and Munch (2002) is that a sh stock can be managed in an evolutionary context by imposing a maximum size limit (all sh above a given size are protected from shing), in addition to the current minimum size limitation. In gill-net sheries such a management option is technically feasible by imposing a maximum mesh size, or in sheries of, e.g. lobster, where the maximum size is limited by the size of the entry to the lobster pot. However no quantitative analysis on whether such a management regime will indeed be benecial has been performed. In this work the role of sheries-induced evolution will be examined via a theoretical model. The model is size-specic and determine the optimal maturation size as a function of the shing pressure. Using quantitative genetics a simple expression for the time-scale of evolution is derived. The model is general and simple, and can be used to obtain a fast but rough indication of the evolutionary pressure on a stock from shing, given von Bertalanffy growth parameters and maturity ogives, which are available for most commercially important stocks. The framework is applied to the Baltic cod stock. This stock experienced a collapse in the 1980s caused by a combination of heavy shing and recurrent recruitment failures (Koster et al., 2003). The collapse does not appear to have been accompanied by a large change in the maturity ogives, neither does there seem to have been a long term trend during the 20th century (Bagge et al., 1994). The questions that will be addressed are: (i) what is the strength of the evolutionary pressure from shing on Baltic cod? (ii) if there is selection towards earlier maturation, are there any options available to reverse or eliminate this pressure? In particular the Conover-Munch conjecture with a refuge from shing for large sh will be examined.

2.1.

Model for life-history

A central ingredient in a life-history model is the specication of growth. Here this is based on the recently proposed framework by West et al. (2001), which can be seen as a generalization of the von Bertalanffy growth model and a special case of dynamic energy budget theory (Kooijman, 2000). This model has the advantage that reproduction is explicitly accounted for. The mass assimilated per time by a sh is fwn . The acquired energy is rst used to cover basal metabolism, which is proportional to the weight, w. If the sh is mature, it additionally routes a xed fraction of its total weight p to reproduction. This leads to growth rates for juvenile and mature individuals of (Fig. 1 a): gj (w) = fwn w, gm (w) = fwn ( + p)w. (1) (2)

For n = 3/4 this corresponds to the growth model by West et al. (2001) and to the one by Lester et al. (2004) if = 0. Total instantaneous mortality rate, Z, is the sum of mortality from predation Zp , shing ZF and from a constant background mortality Z0 . Predation mortality Zp is being imposed by sh larger than their prey. The amount of predators is specied by the size spectrum of all sh which is assumed to be given as a power

2.

Model description

Fishing is mainly size-selective, enforced through a minimum mesh size for trawl and gill nets. Additionally stomach data show that mortality from predation is also size-selective, as smaller sh are more prone to predation (e.g. Sparholt, 1994). Here we calculate tness as a function of the size at maturation, taking into account the size-selective mortality from both predation and shery. Size is represented by the weight of an individual w, but it could just as well be the length l, as these are related through w = al3 , with a = 0.01 g/cm3 .

Fig. 1 (a) von Bertalanffy growth curve (solid), and the tted curve (dashed). The horizontal line is at the current size at maturation. The inset shows the same with logarithmic axes. (b) Size-specic mortality for Baltic cod (solid line) and predation and shing mortalities (dashed lines).

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law with exponent : w , following Thygesen et al. (2005). This effectively leads to a predation mortality (Andersen and Beyer, 2006): Zp (w) = p w1.8 , (3)

tion of size at maturation in the population by (w ), with a mean value w . Selection is acting through the tness function W(w ), such that the selection is (w )W(w )N1 , where N is a normalization factor, N = (w )W(w ) dw . The selection differential S is the difference between the mean value of the size at maturation after and before selection: S = N1
0

where p is a free parameter setting the strength of predation. For an exponent of the size spectrum = 1.8, the predation mortality is independent of size. For > 1.8 predation mortality is decreasing with size, and for = 2.05, the exponent is 1/4. An additional mortality is caused by shing. Fishing is size selective, described by a sigmoidal function with the inection point between no shing and shing at the size wF : ZF (w) = F(1 + exp[(w wF )])
1

w (w )W(w ) dw w .

(7)

(4)

where = 0.01 g1 is a slope parameter and F is the shing mortality for sizes wF (Fig. 1b).

The change in the mean value of a trait from one generation to the next (the selection response) is R = h2 S, where h2 is the heritability. The calculation of R can be operationalized by a few simple assumptions. We assume that (w ) is normal distributed with a mean value w and a standard deviation . To arrive at an analytical approximation of R we make a linearization of the tness around w , so that W(w ) W(w ) + W (w )(w w ), where W (w ) is the derivative of W taken at w . This leads to a simple expression for the selection response: R h2
2W

2.2.

Calculation of tness

(w )

Specication of the proper tness measure depends upon the density dependent effects at work (Mylius and Diekmann, 1995). For most sh stocks the precise nature of the density dependence is not well known. The classical solution is to assume that it takes place early in life (before maturation), and then parameterize it into a stock-recruitment relationship. In that case, the density dependence is not affecting maturation size, and the appropriate tness measure, whose optimum species the evolutionary stable strategy, is the expected lifetime reproductive output (or: how many offspring a female will on average produce during her life), also called R0 (case one in Mylius and Diekmann, 1995). Here it will be called W to avoid confusion with the selection response R to be introduced later. To calculate the tness, the probability of surviving from a size w0 to w is needed:
w

W(w )

(8)

Pw0 w = exp

w0

Z(w) dw , gj (w)

(5)

for the case of a juvenile, and similarly for an adult. Z is the total mortality Z = Zp + ZF + Z0 . A mature female will have a reproductive rate of pw/wp (no. of progeny per time), where wp is the weight of progeny, taken to be 0.001 g and p is the massspecic allocation rate to gonads. The total tness W is the product of the probability of surviving to maturation Pw0 w and the total reproductive output: W(w ) = Pw0 w
w w

This expression formalizes the intuitive result that the selection response is proportional to (1) the heritability, (2) the width of the distribution of w in the population, and (3) the relative slope W (w )/W(w ) of the distribution of tness at the mean of the current size at maturation. A reasonable value of the heritability for maturation in sh is around 0.3 per generation (Law, 2000). It should be mentioned that the use of the breeders equation only applies to stocks with non-overlapping generations. For stocks with overlapping generations, as, e.g. cod, this will lead to an underestimation of negative rates, when the size at maturation is decreasing, due to the fact that early maturing genotypes will appear earlier in the spawning population. The effect will be reversed for positive rates. Care should be taken if a calculation with overlapping generations is performed, iterating many generations ahead, such that the mean size at maturation is changed signicantly. In this case, the result may depend sensitively on the tails of the initial distribution which are hard to estimate reliably. We therefore conne ourselves to examining the initial rate of evolution rst for the current situation and secondly under different management regimes.

2.4.

Properties of the Baltic cod stock

Pw w

pw dw. gm wp

(6)

The optimal size at maturation w is the one which maximizes W(w ), which has to be calculated numerically.

2.3.

Evolutionary rate

An estimate of the rate of the evolution imposed by shing pressure can be calculated by quantitative genetics using the well-known breeders equation. We represent the distribu-

Observations of growth functions are usually reported as ts to the von Bertalanffy growth function, characterized by the maximum length L and the growth parameter K. The von Bertalanffy growth function is identical to the growth functions in (1) and (2) for the value of the exponent n = 2/3. However in the growth model used here the prefactor for the catabolic part of the expression changes at maturation, such that the realized growth is different from von Bertalanffy (although not by much), and dependent upon the size at maturation. Following an idea by Law and Grey (1989), we obtain the values of the growth parameters f, n and from (1) and (2)

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by tting the growth function to the observed von Bertalanffy growth curve, using the current size at maturation and specic allocation rate to gonads p. The von Bertalanffy growth parameters for eastern Baltic cod are approximately K = 0.15 year1 and L = 130 cm (Bagge et al., 1994). In the period 19801989 the 50% maturity ogive was around 3.5 years, corresponding to a weight of 1.5 kg (Bagge et al., 1994). The gonado-somatic index relating the ratio between the weight of gonads and somatic mass was found to be around 0.2 in the same period (Tomkiewicz et al., 1997). Assuming reproduction once a year (thus ignoring skipped spawning), this gives a specic rate of allocation to gonads of p = 0.2 year1 . Fitting the growth curves to the von Bertalanffy curve gave f = 12.4 g1n year1 , n = 0.66 and = 0.23 year1 , and as seen in Fig. 1 a, it is almost indistinguishable from the von Bertalanffy growth curve. To determine the current distribution of size at maturation (w ), we will resort to measured maturity ogives, which determines the fraction of the population which is mature at a given age. Maturity ogives for the period 19801989 (Tomkiewicz et al., 1997) were transfered from age to size using the inverse of the von Bertalanffy growth function. These were then reasonably tted by a normal distribution with 500 g and mean w 1.5 kg. This approach for nding (w ) is simple, but has two caveats: First the observed maturity ogives are maturities for sh with different growth curves, and therefore different places on the age-size reaction norm for maturation. What we are after here is just the distribution corresponding to an average growth rate. However we do not have the data to disentangle these two effects, and must be content with the observation that is therefore probably over-estimated. The rate that we will nd is therefore an approximation of the upper limit of the rate of evolution. The second caveat is that the approach does not take the variation in growth rate before and after maturation into account. We have checked the validity of this by calculating the maturity ogive from the model w as 0 (w )P(w|w ) dw /( 0 (w )P(w|w ) dw ), where P(w|w ) is the probability of being alive at weight w given a size at maturation of w . This distribution was almost indistinguishable from the cumulative distribution of (w ), demonstrating that it is not necessary to account for the change in growth. The predation mortality is determined by the slope of the size spectrum (3). Ursin (1982) showed a spectrum from the Baltic with an exponent around 2.1, which ts well with a recent theoretical estimate predicting an exponent of around 2.05 (Andersen and Beyer, 2006). We have therefore used a slope of = 2.1 and p = 107 g 2 year1 (Fig. 1b). This leads to a predation mortality for a larvae of 1 g of 1.2 year1 , and for a mature individual of between 0.2 and 0.1 year1 , which seems reasonable. Fishing is starting for sh around 1 kg (Kristiansen et al., 2006), and the current level is F = 1 year1 (Bagge et al., 1994).

Fig. 2 Fitness W as a function of the size at maturation for the current situation (thick line) with the current maturation size at the vertical line. The solid lines are calculations where large sh are not subject to shing, beginning at (from bottom to top line): wFend = 10, 7.5 and 5 kg. The dotted curve corresponds to wFend = 10 kg and a shing mortality on large sh of 0.05 year1 . The dashed line is with a selective shing mortality on mature sh of Fm = 1 year1 and a shing mortality on immarture sh of Fj = 0.1 year1 . This tness has been divided by 3 to t it into the current plot. The current maturation distribution (w ) is illustrated with the grey patch.

3.

Results and interpretation

The tness curve as a function of size was calculated numerically from (6) (Fig. 2). The slope around the current situation is negative, showing an evolutionary pressure for lowering the maturation size. The evolutionary selection response calculated was 36 g/generation under a shing mortality of F =

1 year1 . This rate can also be expressed in the units of Haldanes by normalizing with the standard deviation, leading to an evolutionary rate of 0.072 Haldanes. The rate of evolution weakens at an almost linear rate to zero near F = 0.12 year1 (Fig. 3a). This shows that the high shing pressure is responsible for the current evolutionary pressure. Our present-day rate is similar to those estimated for other sh stocks (Law and Rowell, 1993; Kinnison and Hendry, 2001), but is smaller than empirical estimates for north-west Atlantic cod (Olsen et al., 2004). The optimal maturation size w was calculated numerically as a function of shing mortality (Fig. 4). In particular, for present conditions (F 1 year1 ), we found an optimum of close to 50 g, which is very much smaller than presently observed in eastern Baltic cod (w 1.5 kg; Tomkiewicz et al., 1997). Multivariate sensitivity testing using the three main variables showed our calculation to be a robust estimate of optimal maturation size (the range being 300 g and below), illustrated by shading in Fig. 4. The selection pressure means that the current size at maturation is not optimal. Only for very small shing mortality is the current size at maturation optimal. If shing is totally absent, we predict optimal maturation size to be 5 kg. At a shing mortality of around 0.1 year1 there is a discrete shift in the optimal size at maturation caused by a switch between two local maxima of the tness function (Taborsky et al., 2003). The rst of these is associated with early spawning to ensure at least some progeny before possible death by shing. The second maximum is associated with small sh which experience larger predation mortality; they maximise their growth rate to escape this and thus postpone spawning (Abrams and Rowe, 1996). With larger shing mortality the strategy of post-poned spawning is not viable, since shing removes the size refuge. As growth continues after

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Fig. 3 The selection response R for two situations: (a) the current situation as a function of the shing mortality F and (b) for the situation with a reserve for large sh, as a function of the maximum size which is shed wFend . The thick line is from a numerical calculation of R, the dashed line is the analytical approximation in (8) and the dotted vertical line is the current shing pressure. maturation, the sh has to mature before hitting the wall of shing mortality that starts around 1 kg, so the optimal size is depressed below this, resulting in the surprisingly small value. It is relevant to question the validity of the surprisingly small predicted value of optimal size at maturation. There are two reasons why this prediction should be treated with caution: (1) the maximum in the tness is not very pronounced, so the actual value of the maximum is not well dened; (2) if there is such a large change in size at maturation as indicated, we can not expect that our hypothesis of the density dependence hold any longer. In particular growth compensation will play a role. Since shing has persisted for several decades near present levels, one may ask why maturation size has not yet reached its optimal value. Answering this question starts with an estimate of the pre-shing optimal maturation size, which we see from Fig. 4 may have been any value greater than 1 kg. There is evidence that the stock was shed as far back as 1400s, when there was additionally predation from a large stock of marine mammals (MacKenzie et al., 2002). Total mortality (predation plus shing) on large sh could therefore easily have been greater than the 0.1 year1 , which as Fig. 4 shows, is the threshold for downward evolution of maturation size. Although uncertainty persists in this argument, we may deduce that either downward evolution is still progressing, but at a rate that has always been slow, or that there are physiological or behavioural limits to maturation size, not accounted for. In the north-east Arctic cod the limiting mechanism is a costly spawning migration (Jrgensen and Fiksen, 2006), which is particularly expensive for small sh, as they cannot reach the energetically optimal cruising velocity (Ware, 1978). As the spawning migration in the Baltic is small (on the order of 100 km), this is unlikely to explain the difference between observed and optimal sizes. For Baltic cod an explanation could be that the sh do not eat during spawning, which can be approximately modelled by an increase in the cost of spawning p. Increasing this parameter delays maturation, but even a factor of two increase does not lead to a substantial increase. Other possible candidates include the fact that older sh tend to produce eggs and larvae with higher survival rates (MacKenzie et al., 1998), which would raise the lower limit for optimal maturation size. Another possibility is that due to discrete annual spawning, maturation size is caught in an evolutionary strategy, and may not be able to change to an evolutionary regime with earlier reproduction (de Roos et al., 2006). Finally it should be noted that the successful reproduction of Baltic cod rely on intermittent inows of oxygenated water from the North Sea. Lack of inows can lead to several years of reproduction failure. Such events could benet larger cod, which would lead to a selection gradient in the opposite direction of what is predicted here. A previous analysis of the evolutionary response of cod to exploitation found a very weak evolutionary response (Martinez-Garmendia, 1998). The reason for that result appears to be rooted in an unjustied coupling between fecundity (corresponding to our parameter p) and maturation size, such that earlier maturing genotypes apparently have a lower fecundity.

3.1.
Fig. 4 Optimal maturation size w as a function of the shing mortality for Baltic cod. The two dashed lines are the current w and F, respectively, and the black circle is therefore the current situation. The grey area represents results from calculations of w , with the main parameters chosen at random in the ranges: p [0.1, 0.3]; start of shing wF [750 g, 2500 g]; p [0.5 107 , 2 107 ]; f varying between 0.75 and 1.5 of its base value.

Management options

We conceive three management options in response to the evolutionary pressure from shing: (a) to reduce shing mortality below 0.1 year1 , (b) to enforce a shing regime where only mature sh are targeted, or (c) to make a reserve for large sh (Conover and Munch, 2002). The rst option effectively means closure of the shery. The second option is interesting, as shing selectively on the mature population was the traditional practice for the

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north-east Arctic cod, as mainly the spawning stock was accessible for shery (Law and Grey, 1989). Such a management scheme can be implemented in the model framework by setting the general level of shing mortality equal to the juvenile shing mortality F = Fj , and adding an extra mortality term corresponding to the shing mortality on mature sh Fm Fj (Fm being the shing mortality on mature sh) in the calculation of the survival probability for mature sh in (6). We tested this option by setting juvenile shing to 0.1 year1 and mature shing to 1.0 year1 . This led to a tness curve with a weakly positive slope around the current size at maturation, demonstrating that concentrating the shing on mature stocks eliminates the evolutionary pressure from shing (Fig. 2). The exact location of the optimal size at maturation in this case is dependent on the constant background mortality Z0 . This result is consistent with the life-history theory which has established that harvesting only mature individuals selects for later maturation (Law and Grey, 1989; Roff, 1992). Finally we tested the option of saving large sh by imposing a zero shing mortality for sh larger than a given size wFend . The main result was that a second maximum associated with late spawning was created. Depending upon the maximum size which is available for the shery, that maximum may even be the optimum strategy (wFend < 5.5 kg). There are a number of caveats: rst of all, the newly created optimum is separated from the current situation by a trough in tness, possibly leaving it inaccessible to incremental quantitative evolution. To change the direction of evolution, the selection response has to change sign, which happens only when sh larger than just 4 kg are not subject to shing (Fig. 3b). Leaving those sh out of the shery does not appear to be a politically acceptable option. Another problem is that the magnitude of the maximum associated with late spawning is quite sensitive to the value of the background mortality. This also means that only a modest shing mortality on the larger sh will make the evolutionary advantage of late spawning disappear, e.g. with a shing mortality on large sh of just 0.05 year1 the tness optimum at late maturation disappears (Fig. 2, dotted line). Taken together, removing shing of large sh does not seem to be an attractive management option to reverse the current situation, but it may be used as an option to preserve the size at maturation for an already healthy stock.

4.

Conclusions

The typical approach for modelling sh populations is via an age-based approach (e.g. Xiao, 2000), as this is mathematically simple. However, most ecological interactions (i.e. predation mortality) and shing mortality is related to size, not age. A recently popular approach is the use of individual-based models, where the size-specic nature of the interactions are easily handled (e.g. Martinez-Garmendia, 1998). These have the advantage that detail can easily be added, but the disadvantage that they require computer simulations and their inherent complexity may mask the salient features of the process under study. The framework presented here is sizespecic, yet it is simple to apply. In particular it only uses parameters which are easy to estimate from existing knowl-

edge available for many exploited stocks. The framework therefore provides a fast method to get an indication of the selection pressure on a given stock, just given von Bertalanffy growth parameters and maturity ogives. The simple expression for the selection response R in (8) seems to be a good approximation for the full numerical solution (Fig. 3). Due to the simplicity of the framework, it contains a number of limitations, which should be kept in mind: (1) the density dependence is simple, in particular it does not contain growth compensation and (2) the determination of the distribution of size at maturation from the maturity ogives is not perfect. Particularly the width of the distribution is over-estimated as the phenotypic variation is not disentangled from the genotypic variation. This over-estimation of the selection response may to some extent be countered by the assumption of nonoverlapping generations. The results show that sheries-induced evolution is likely to be persistent in Baltic cod, especially given the predicted ineffectiveness of all but the most drastic management measures. The large distance between optimal and realised maturation size may imply sub-optimal productivity due to sub-optimal tness as the tness landscape has changed faster than the sh can adapt, leading to reduced sustainable yields (Conover and Munch, 2002). The results highlight important gaps in our knowledge about evolution of maturation size. It remains unclear whether maturation size in Baltic cod is subject to a lower limit and if so, what causes this. An important unanswered question is why the rates of evolution found in some collapsing stocks (Olsen et al., 2004) are so much greater than we predict for the relatively stable Baltic cod? Sensitivity analysis against the main parameters used in the calculations showed insufcient scope to account for the difference between our predictions and evolutionary rates observed in collapsing stocks. However, the assumptions of the basic breeders equation may not hold in a rapidly changing and stressed population. In particular the heritability may not remain constant (Hoffmann and Merila, 1999) and non-additive genetic variance may add to the broad-sense heritability (Blows and Hoffmann, 1996); such components of inheritance are not accounted for in the simple model (Heywood, 2005). Furthermore, the effect of overlapping generations will have an effect which would increase the downward speed of evolution. There are therefore several reasons, that have yet to be examined, why evolution may be accelerated in an overexploited population. The analysis we used could provide a baseline, by predicting evolution in a relatively benign environment, for comparison with populations in crisis. The question, then, is not so much why Baltic cod are evolving so slowly in response to shing pressure, but why some other populations seem to evolve so fast.

Acknowledgements
We thank Brian MacKenzie for information about the Baltic ecosystem. The present analysis is a contribution to the EU FP6 Specic Targeted Research Projects 022717 (UNCOVER) and the European Network of Excellence for Ocean Ecosystems Analysis 511106-2 (EUR-OCEANS).

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