ICES CM 2009/(F:02)

Modeling the competition for food by in the under varying climate regimes and fishing pressures.

Van Kooten, T. 1, Van der Zon, S. 1, Van Hal, R. 1, Hille Ris Lambers, R. 1, Hintzen, N.T. 1, Rijnsdorp, A.D. 1,2

1Wageningen IMARES, Institute for Marine resources and Ecosystem Studies, P.O. Box 68, 1970 AB IJmuiden, the Netherlands. 2Aquaculture and Fisheries group, Wageningen University, P.O. Box 338, 6700 AH Wageningen, the Netherlands

Abstract

A clear increase in average water temperature has been observed in recent decades in the North Sea. Simultaneously, a number of small demersal fish species like scaldfish (Arnoglossus Laterna ) and solenette ( Buglossidium luteum ) have increased strongly in abundance in regions which were previously considered to be outside their temperature range. These species compete for resources with exploited flatfish populations such as ( Pleuronectes platessa) , which can potentially lead to reduced availability of valuable flatfish resources. We develop a stage-structured model to study how the competition between these groups plays out under different scenarios of harvesting and climate change.

Keywords: Food web model; Competition; Temperature; Fisheries; Flatfish

Contact author: Tobias van Kooten, Wageningen IMARES (Inst. for Marine Resources & Ecosystem Studies) P.O. Box 68, 1970 AB Ijmuiden, The Netherlands E- mail: [email protected]

1 ICES CM 2009/(F:02)

Introduction

The mean surface temperature of the North Sea has increased by 1.5 °C over a period of 25 years since 1980 (Philippart et al. 2007). Such warming has been associated with many ecosystem effects, one of which is a shift in species’ distributions and relative abundances, as the geographic boundaries of their preferred temperature range shift to higher latitudes and deeper waters (Beare et al. 2004; Dulvy et al. 2008; Perry et al. 2005). Because marine species differ in their temperature tolerance, species range shifts and changes in abundance in response to temperature are likely to lead to changed trophic interactions (Rijnsdorp et al. 2009). Many of the fish species in the North Sea are heavily exploited (ICES 2008), and to ensure proper management of these species, it is important to assess how climate- induced changes in species interactions affect their production and distribution. One of the important exploited species in the North Sea is plaice (Pleuronectes platessa), the abundance of which has decreased in the last decades. This is often attributed to overexploitation, but other factors do seem to play a role (ICES 2008). Theoretically, the reduction in abundance should lead to increased per capita food availability, and hence faster growth for the remaining plaice. However, plaice growth has slowed down over the years (Rijnsdorp et al. 2004), suggesting that either the production of the benthic invertebrates on which plaice feeds has decreased, or that a larger fraction of potential plaice food is consumed by other species in the community. One candidate for such resource competition is solenette ( Buglossidium luteum ), which has a substantial diet overlap with plaice (Amara et al. 2004; Piet et al. 1998). Although solenette has always been present in the North Sea, the recent seawater warming has coincided with a large increase in this species’ abundance (Tulp et al. 2008, van Hal et al., in press) It is estimated that solenette may currently use up to 35% of benthic primary production in the central North Sea (Jennings et al. 2008). This production could otherwise have been used by harvestable fish species. Here, we explore the hypothesis that the observed increase in solenette abundance is responsible for the observed decline of plaice in the North Sea. We construct a dynamical model of the plaice-solenette system in which plaice adults compete for food with solenette.

2 ICES CM 2009/(F:02)

Model

We use a recently developed framework for modeling the biomass of size-structured populations (de Roos et al. 2008b) which discretizes the population size distribution into a fixed number of stages. The dynamics of these models are identical to more complex fully size-structured models under equilibrium conditions. These models have been used to study predator-prey interactions and more complex community assemblages (de Roos et al. 2008a; de Roos et al. 2007), but have so far not been employed in relation to resource competition. We divide plaice life history into a juvenile ( J ) and an adult ( A ) stage, and treat solenette ( S ) as an unstructured population (Figure 1). Adult plaice and solenette share the same resource ( R ), while juvenile plaice are assumed to be geographically separated and have an exclusive resource ( RJ , which for simplicity is assumed constant). This formulation reflects the contrasting ecology of the two species, as plaice utilizes shallow coastal waters as nursery grounds and offshore waters as adults (Rijnsdorp and van Beek 1991), while solenette uses offshore waters both as juveniles and adults (Baltus and Van der Veer 1995).

Solenette Adult Plaice [A] [µ ] [µ ] S [S] A

Maturation [γ(vj(R))] Reproduction [v a(R)]

Growth [vS(R)] Juvenile Plaice [J] [µj]

Growth [vA(R)] Growth [vj(R J)]

Shared resource Juvenile plaice

[R] resource [R J]

Figure 1:Schematic representation of the plaice-solenette interaction described in equations (1). See main text for explanation of symbols.

This system is described by the system of ordinary differential equations:

3 ICES CM 2009/(F:02)

dR (q A + q S)⋅ I ⋅ R = δ ⋅ ()R − R − A S dt max H + R dJ = ⋅ + ()− γ − µ ⋅ v A (R) A vJ J J dt (1) dA = γ ⋅ J − µ ⋅ A dt A dS = ()v (R) − µ ⋅ S dt S S In absence of consumers, the resource R follows semi-chemostat dynamics with δ maximum density Rmax and inflow rate . It is consumed by adult plaice ( A ) and solenette ( S ) according to a type II functional response, with mass-specific maximum attack rate I and half saturation constant H . The parameters qS and q A scale the maximum attack rate of solenette and adult plaice, and determine their relative competitiveness (see discussion in de Roos et al. 2007 and below). Solenette die at µ density-independent mortality rate S , and grow according to q ⋅σ ⋅ I ⋅ R ν (R) = S − T , (2) S H + R Where T is the mass-specific metabolic rate, and σ is a conversion efficiency. The right hand side of equation (2) gives the net biomass increase as a result of feeding (or decrease when resource availability is insufficient to cover metabolic costs), as the intake of biomass minus the ‘cost of living’. For plaice, each of the stages J and A have a similar function. Growth of adult plaice is given by q ⋅σ ⋅ I ⋅ R ν (R) = A − T . (3) A H + R All biomass accumulation of adult plaice is assumed to be used for reproduction, and ν ⋅ adult somatic growth is assumed negligible, hence the term A (R) A in the equation for dJ /dt , and the absence of such a term in the equation for dA /dt in system (1).

Juvenile plaice feed on their own (constant) resource, RJ , and grow according to ν = σ ⋅ ⋅ − J I RJ T . Maturation of juvenile plaice into the adult stage is described by v − µ γ = j J µ 1− J 1− z vJ Where the parameter z is the ratio of the mass of an individual entering the juvenile stage to the mass of an individual in the adult stage. The function γ is the unique

4 ICES CM 2009/(F:02) feature of this class of models, and it is derived such that the model equilibria correspond to those of a fully size-structured model (de Roos et al. 2008b). Note that ν ν the growth functions A (R) and S(R ) can become negative under starvation conditions, when resource intake is insufficient to cover metabolism, T . For solenette, this means biomass loss through starvation, but for plaice, it results in biomass loss of the juvenile stage due to starvation of adults. This illustrates that the model is valid only under equilibrium conditions.

Parameters

Table 1: Default values of model parameters Parameter Symbol Value Unit Resource growth rate δ 0.1 d-1

Maximum resource abundance Rmax 2.0 g

Juvenile plaice resource abundance RJ 1.0 g Maximum intake rate I 0.15 d-1 Metabolic rate T 0.0055 d-1 Half-saturation constant H 0.5 g Recruit per ratio r 0.006 - Assimilation efficiency σ 0.8 -

Adult plaice competitive scaling q A 1.0 -

Solenette competitive scaling qS 1.0 - Plaice juvenile-to-adult mass ratio z 0.001 - µ -1 Juvenile plaice mortality J 0.01 d µ -1 Adult plaice mortality A 0.03 d µ -1 Solenette mortality S 0.01 d

The values of all parameters are given in Table 1. It is important to note that in simple models such as (1), precise parameter estimates become less important, as the aims of this study are to understand qualitative transitions, rather than quantitative predictions precise shifts. Parameters were therefore chosen to loosely describe flatfish. Here we discuss only a few parameter values. The maximum per unit weight intake rate was calculated for plaice from (Fonds et al. 1992). Maximum ingestion of plaice feeding on mussel meat was calculated as ~1.5 mg ash free dry weight (AFDW) per gram fish AFDW. Bivalva represent an approximate 5.5 g wet weight (WW) per g AFDW (Ricciardi and Bourget 1998), one unit plaice AFDW represents approximately 5 units WW (Fonds et al. 1992). This leads to a maximum intake of 0.09 g mussel meat per g

5 ICES CM 2009/(F:02) plaice per day. Since most prey species have a higher water content than mussel meat, we assume a maximum intake rate of 0.15 d -1. We use the volume-specific maintenance rates for plaice published in Rijnsdorp & Ibelings (1989), (20 J cm -3 d-1), which, using the energy content and AFDW-WW conversion for , -1 amounts to 0.055d . The recruit per egg ratio r was calculated by dividing the adult offspring production by the weight of a plaice egg, multiplying by the fraction of that survive the egg and larval phase, and then multiplying by the mass of a recruit to -1 the juvenile plaice stage : this amounts to 0.006d .

Results

In our model, coexistence between plaice and solenette is not possible (Figure 2). This is because the outcome of the competitive interaction is determined by which species induces the lowest equilibrium resource density. Coexistence is possible only in the highly unlikely case that these densities are exactly equal among the two species. Even the presence of an exclusive and inexhaustible resource, for juvenile plaice does not alter this principle: Adult plaice can’t reproduce when resource abundance is such ν ≤ that A (R) 0 (eq. (3)) and in absence of reproduction, no plaice population can persist. The equilibrium density of the shared resource R depends in a complex way on a number of parameters. We used numerical bifurcation analysis (Kuznetsov 1998) to study the outcome of competition in relation to several key parameters.

Increasing the competitiveness of solenette allows it to take over the system and drive plaice to extinction (Figure 2). The exact value of competitiveness for which the shift µ occurs depends strongly on the mortality rate of adult plaice ( A ), which includes fishing mortality and hence its value can be interpreted as a proxy for fishing intensity. The mortality of adult plaice strongly affects the equilibrium biomass of adult plaice ν ⋅ but also that of juvenile plaice, since the total reproductive output, A (R) A , depends on the adult density. Increasing adult mortality from low values (compare Figure 2, left panel and middle panel), the equilibrium juvenile density increases as the reduction in adult biomass A is more than compensated for by the increased per ν unit biomass production A (R) ; leading to an increased total reproductive output ν ⋅ A (R) A . When mortality is increased beyond some threshold, the adult biomass

6 ICES CM 2009/(F:02) reduction can no longer be compensated for by the higher per unit biomass production, and both juvenile and adult densities are now reduced by adult mortality (compare Figure 2, middle panel and right panel).

The increase in equilibrium solenette density with qS at intermediate and high plaice mortality occurs because the parameter qS scales the maximum attack rate of solenette. When it increases, solenette simply becomes a more efficient feeder. This can lead to higher equilibrium density, as a larger proportion of resource production is converted into solenette biomass. At high qS , this effect is reduced as resource productivity, rather than feeding efficiency becomes the limiting factor, and the µ equilibrium biomass of solenette levels off. When A is low (Figure 2, left panel), the range of qS values where this occurs are in the plaice-dominated range of parameter space.

Figure 2: Effect of varying solenette competitiveness (qS) on equilibrium biomass abundance of plaice(J, black line, A, blue line) and solenette (S, red line), for 3 values of adult plaice mortality. At very high solenette competitiveness, plaice is unable to persist in the system. The parameter range where plaice can persist decreases with increasing adult plaice mortality. The lack of overlap between the plaice and solenette parameter ranges illustrates the lack of coexistence. All other parameters as in Table 1.

When adult plaice mortality and/or solenette competitiveness is high, plaice cannot persist (Figure 3, the drawn black line indicates where the switch between the species µ occurs). Plaice furthermore has a maximum A , above which it cannot persist even when solenette abundance is kept at zero. Similarly, solenette has a minimum qS ,

7 ICES CM 2009/(F:02) below which it always goes extinct. Where these regions overlap, no fish species can persist. This result is qualitatively independent of the conditions in the plaice juvenile , although a higher productivity ( RJ ) does increase the scope for persistence of plaice (Figure 4). The same applies to juvenile plaice mortality, but in the opposite direction: lower mortality causes the same shift of the invasion boundary as higher productivity (result not shown).

Figure 3:Outcome of the competitive interaction for combinations of the parameters qS (solenette competitiveness) and µA (adult plaice mortality). At high µA, plaice can not persist even in absence of solenette. Similarly, at low qS, solenette can not persist even in absence of plaice. The region marked ‘no fish’ delineates where these parameter regions overlap.

8 ICES CM 2009/(F:02)

Figure 4: The effect of changing the productivity of the plaice nursery grounds on the competition between plaice and solenette. The figure is the same as Figure 3, but with the invasion boundary (thick black lines) drawn for 3 different values of Rj, the productivity of the plaice nursery grounds. It shows that higher resource productivity for juveniles helps plaice to persist under higher mortality and to withstand stronger competition.

Although our model is stage-structured and hence has no explicit individual growth functions, we can use the equilibrium resource density as a general measure for individual growth rate. While an increase of fishing intensity, in the form of plaice adult mortality, increases the equilibrium resource level, and hence individual growth rate, the effect of solenette is to strongly decrease it (Figure 5). The ‘average’ equilibrium density over a range of solenette competitiveness decreases with plaice adult mortality, because the range of qS values where plaice wins the competition decreases with increasing adult mortality.

9 ICES CM 2009/(F:02)

Figure 5: Equilibrium resource densities corresponding to the equilibria drawn in figure 2. To the left of each solid dot plaice is present, to the right solenette is. The resource density in the plaice equilibrium increases with µA , while the equilibrium density in the solenette equilibrium strongly decreases with solenette competitiveness qS.

Discussion

Our model predicts that plaice and solenette cannot persist together. Although our results are in line with the classical competitive exclusion principle (Gause 1934), which states that no more than one population can persist on a single limiting resource, ecosystems in nature are affected by stochasticity, seasonality, life history complexity, spatial heterogeneity and many other complicating factors, each of which alone could prevent the occurrence of competitive exclusion. We have deliberately omitted all this complexity in our choice of model, because our aim is to provide a basis for

10 ICES CM 2009/(F:02) discussion, rather than to correctly predict the outcome of the plaice-solenette interaction on a North Sea-wide scale.

If we think of the outcome of competition as a highly local process, and the North Sea as a complex and dynamic collection of microhabitats which cause the competitiveness of the species to vary strongly depending on their location, then the range of qS values over which plaice persists (in figure 2) can be seen as the subset of microhabitats that favor plaice, while solenette is favored in the rest. Under this interpretation, the panels in figure 2 show that increased fishing intensity on adult plaice increases the range of microhabitats where solenette will outcompete plaice, and so reduces potential plaice production. Similarly, figure 3 shows that at very low plaice adult mortality, solenette only persists in microhabitats which are strongly favorable. Furthermore, a reduction in fishing pressure (adult plaice mortality) will not necessarily help plaice: if solenette competitiveness is high enough, adult plaice mortality has only a limited effect on the outcome of competition. However, it can increase the density of adult plaice in those microhabitats where plaice is the superior competitor (Figure 2). Along this line of interpretation, figure 5 indicates that although the resource density, and hence growth of adult plaice, does increase with increased fishing intensity, this effect is possibly (over-) compensated by a strong decrease in resource density caused by the simultaneously increased dominance of solenette and the much reduced resource density in the microhabitats where solenette dominates. Hence, it can be argued that our model predicts increased solenette abundance, reduced adult plaice density and reduced growth of plaice in response to increasing fishing mortality and/or climate change. This is a new hypothesis explaining existing data, which requires further analysis of both data and models.

The results we present here are clearly consistent with common sense: If one species is ‘helped’ by changing its parameter values, it becomes less prone to be outcompeted by the other. However, even this simple model has led to a sharpened hypothesis regarding the relation between increases plaice exploitation and the advance of solenette in the North Sea. This illustrates the potential of using simple models to evaluate, in a qualitative sense, the consequences of certain hypotheses. The model we have used here can be readily expanded to incorporate more complexity, which would

11 ICES CM 2009/(F:02) increase the potential for counterintuitive results. We sketch a few directions in which this model can be extended. Currently, we have assumed a 100% food overlap between solenette and adult plaice. We could introduce an exclusive resource for each, which forms an alternative energy source. Classical competition theory predicts that as long as both species cannot persist without the shared resource, competitive exclusion occurs. Coexistence can occur only when at least one of the species can survive without the shared resource. Even with complete food overlap between adult plaice and solenette, this food source consists of many species and is strongly heterogeneous. It is likely that solenette and plaice have different foraging capacities on different components of the shared resource. For example solenette may be more efficient than plaice in feeding on bivalves, while plaice may be better equipped for feeding on polychaetes. Such specializations within the spectrum of shared prey can potentially induce coexistence. Another extension would be to include density- dependence in the juvenile stage of plaice. This allows for food-dependent maturation, potentially leading to a wealth of non-linear effects, particularly in response to size- dependent harvesting (van Kooten et al. 2005; van Kooten et al. 2007). Alternatively, a 3 rd stage of plaice could be included, representing very large plaice that move far north and to deep waters where persistence of solenette is impossible so that no competition occurs. There are also spatial considerations that could lead to extensions of the model. The geographic ranges where solenette and plaice occur do not overlap completely. It may be that the population in the overlapping area survives as a result of immigration from areas where only one of the species exists.

We have used the parameter qS , a property of solenette, to vary competitive strength of the two species, while holding plaice competitiveness constant. However, the outcome of the interaction depends on the relative competitiveness of solenette versus plaice, and climate change is unlikely to affect one species but not the other. Solenette and plaice appear to have similar temperature requirements (Dulvy et al. 2008). If the direct effects of increased temperature, that is, the effects on physiological rates, are similar for the two species then the decisive factor in competition is likely one of the indirect effects. Further elaborations of the model can be developed and explored to narrow down which one.

12 ICES CM 2009/(F:02)

Acknowledgements

This research is part of the strategic research program "Sustainable spatial development of ecosystems, landscapes, seas and regions" and is funded by the Dutch Ministry of Agriculture, Nature Conservation and Food Quality.

References

Amara, R., K. Mahe, O. LePape, and N. Desroy. 2004. Growth, feeding and distribution of the solenette Buglossidium luteum with particular reference to its habitat preference. Journal of Sea Research 51:211-217. Baltus, C. A. M., and H. W. Van der Veer. 1995. Nursery areas of solenette Buglossidium luteum (Risso, 1810) and scaldfish Arnoglossus laterna (Walbaum, 1792) in the southern North Sea. Netherlands Journal of Sea Research 34:81-87. Beare, D. J., F. Burns, A. Greig, E. G. Jones, K. Peach, M. Kienzle, E. McKenzie et al. 2004. Long-term increases in prevalence of North Sea fishes having southern biogeographic affinities. Marine Ecology-Progress Series 284:269-278. de Roos, A. M., T. Schellekens, T. Van Kooten, and L. Persson. 2008a. Stage-specific predator species help each other to persist while competing for a single prey. proceedings of the National Academy of Sciences of the USA 105:13930- 13935. de Roos, A. M., T. Schellekens, T. van Kooten, K. van de Wolfshaar, D. C. Claessen, and L. Persson. 2007. Food-dependent growth leads to overcompensation in stage-specific biomass when mortality increases: the influence of maturation versus reproduction regulation. American Naturalist 170:E59-E76. de Roos, A. M., T. Schellekens, T. van Kooten, K. E. van de Wolfshaar, D. Claessen, and L. Persson. 2008b. Simplifying a physiologically structured population model to a stage-structured biomass model. Theoretical Population Biology 73:47-62. Dulvy, N. K., S. I. Rogers, S. Jennings, V. Stelzenmuller, S. R. Dye, and H. R. Skjoldal. 2008. Climate change and deepening of the North Sea fish assemblage: a biotic indicator of warming seas. Journal of Applied Ecology 45:1029-1039.

13 ICES CM 2009/(F:02)

Fonds, M., R. Cronie, A. D. Vethaak, and P. Vanderpuyl. 1992. Metabolism, Food- Consumption and Growth of Plaice (Pleuronectes-Platessa) and (Platichthys-Flesus) in Relation to Fish Size and Temperature. Netherlands Journal of Sea Research 29:127-143. Gause, G. F. 1934, The struggle for existence, Williams & Wilkins Co., Baltimore, USA. ICES. 2008. Report of the Working Group on the Assessment of Demersal Stocks in the North Sea and Skagerrak - Spring and Autumn(WGNSSK), 1-8 May ICES Copenhagen and By Correspondence. Diane. 960 pp. Jennings, S., R. van Hal, J. G. Hiddink, and T. A. D. Maxwell. 2008. Fishing effects on energy use by North Sea fishes. Journal of Sea Research 60:74-88. Kuznetsov, Y. A. 1998, Elements of applied bifurcation theory. New York, Springer Verlag. Perry, A. L., P. J. Low, J. R. Ellis, and J. D. Reynolds. 2005. Climate change and distribution shifts in marine fishes. Science 308:1912-1915. Philippart, C. J. M., R. Anadón, R. Danovaro, J. W. Dippner, K. F. Drinkwater, S. J. Hawkins, G. O'Sulivan et al. 2007. Climate change impacts on the European marine and coastal environment, Marine Board–ESF Position Paper. Piet, G. J., A. B. Pfisterer, and A. D. Rijnsdorp. 1998. On factors structuring the flatfish assemblage in the southern North Sea. Journal of Sea Research 40:143-152. Ricciardi, A., and E. Bourget. 1998. Weight-to-weight conversion factors for marine benthic macroinvertebrates. Marine Ecology-Progress Series 163:245-251. Rijnsdorp, A. D., L. J. Bolle, and O. A. Van Keeken. 2004. Changes in productivity of the southeastern North Sea as reflected in the growth of plaice and . ICES CM2004/K:13. Rijnsdorp, A. D., and B. Ibelings. 1989. Sexual dimorphism in the energetics of reproduction and growth of north-sea plaice, pleuronectes-platessa L. Journal of Fish Biology 35:401-415. Rijnsdorp, A. D., M. A. Peck, G. H. Engelhard, C. Mollmann, and J. K. Pinnegar. 2009. Resolving the effect of climate change on fish populations. ICES J. Mar. Sci. 66:1570-1583.

14 ICES CM 2009/(F:02)

Rijnsdorp, A. D., and F. A. van Beek. 1991. Changes in Growth of Plaice Pleuronectes-Platessa L and Sole Solea-Solea (L) in the North-Sea. Netherlands Journal of Sea Research 27:441-457. Tulp, I., L. J. Bolle, and A. D. Rijnsdorp. 2008. Signals from the shallows: In search of common patterns in long-term trends in Dutch estuarine and coastal fish. Journal of Sea Research 60:54-73. van Kooten, T., A. M. de Roos, and L. Persson. 2005. Bistability and an Allee effect as emergent properties of stage-specific predation. Journal of Theoretical Biology 237:67-74. van Kooten, T., L. Persson, and A. M. de Roos. 2007. Size-dependent mortality induces life history changes mediated through population dynamical feedbacks. American Naturalist 170:158-170.

15