Predation-mediated recruitment in the Georges Bank fish community

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1 ICES Journal of Marine Science, 58: doi:1.16/jmsc , available online at on Predation-mediated recruitment in the Georges Bank fish community T. S. Tsou and J. S. Collie Tsou, T. S., and Collie, J. S. 21. Predation-mediated recruitment in the Georges Bank fish community. ICES Journal of Marine Science, 58: Understanding the mechanisms that control recruitment in marine fish populations is important for conservation and also for more efficient management through improved predictions of abundance. We examined the role of predation in regulating recruitment by applying multispecies virtual population analysis (MSVPA) to eight fish species on Georges Bank. Cod and silver hake were the most important predators and herring and silver hake were the most important prey species. Predation on cod and silver hake was compensatory, because cannibalism was the dominant source of predation for these species. Predation on herring and mackerel appeared to be slightly depensatory or density-independent. Predation on young fish also affected the relative cohort size at age 2. Therefore, predation should be considered when making medium- to long-term recruitment forecasts. 21 International Council for the Exploration of the Sea Keywords: Georges Bank, MSVPA, predation, recruitment. Published electronically 1 August 21. T.-S. Tsou and J. S. Collie: Graduate School of Oceanography, University of Rhode Island, Narragansett, RI 2882, USA. Present address T.-S. Tsou: Florida Marine Research Institute, 1 8th Avenue SE, St. Petersburg, FL 3371, USA; Tel: ; fax: ; Introduction Predation among exploited fish species contributes significantly to their natural mortality and varies from year to year (Pope, 1991). The magnitude and the variability of predation on young fish play an important role in regulating species abundance in many marine ecosystems (Bax, 1991). Therefore, understanding how species interact is essential for making long-term predictions about multispecies fisheries. In the North Sea, for example, decreasing the fishing mortality on cod, haddock, whiting, and saithe would have the contraintuitive result of reducing overall yield because of increased predation (Pope, 1991). The combined effects of fishing and predation can be estimated with multispecies virtual population analysis (MSVPA), which provides useful insight into the role of predator prey interactions by quantifying the food consumption of major predators (Sparre, 198). MSVPA simultaneously estimates fishing and predation mortality by year and age group for any number of predator and prey species on the basis of catch-at-age and stomach-content data. MSVPA also estimates (constant) predator prey suitability coefficients, which can be used to forecast predation under varying abundance of predators and prey. In MSVPA, natural mortality is a function of predation. This is a significant departure from the singlespecies philosophy, which generally assumes constant natural mortality over all age groups and years (or a constant natural mortality age-array over all years). To this end, natural mortality is partitioned into predation mortality and residual natural mortality caused by other factors. is a dynamic function of predator consumption, predator preference, predator abundance, and prey abundance, and is considered to be the dominant source of mortality on young fish (Sparre, 1991). The residual mortality is usually treated as a constant and is considered to be much lower than predation mortality. Predation was identified as the largest source of mortality of pre-recruit fish on Georges Bank (Sissenwine et al., 1984), which is considered to be a predator-controlled ecosystem (Sissenwine, 1986; Overholtz et al., 1991). As part of the Coastal Ocean Program, Georges Bank predation study, we applied MSVPA to estimate predation mortality and to reconstruct the abundance-at-age of six important fish species (for details, see Tsou and Collie, 21). Here, our focus is the role of predation on young fish with respect to recruitment /1/ $35./ 21 International Council for the Exploration of the Sea

2 Predation-mediated recruitment in the Georges Bank fish community 995 Male dogfish Female dogfish Winter skate Haddock Materials and methods Silver hake MSVPA integrates the suitability concept of Andersen and Ursin (1977) for describing predator prey relationships with the traditional form of virtual population analysis (VPA). Sparre (1991) outlines the five basic equations of MSVPA. The first two equations represent the well-established basis for single-species VPA (Gulland, 1965), except that the natural mortality by age group is partitioned into predation mortality and residual natural mortality. can be estimated from the other three equations, which involve biomass-at-age of all species, ingestion ratesat-age for all predators, prey and predator-specific suitability indices (based on stomach content data for individual years or averages over a period), and some estimate of other food (not represented by the modelled species). Following the approach of Sparre (198), we assumed a constant biomass of the ecosystem, such that the expected changes in other food compensate for changes in the abundance of exploited prey. The total biomass of fish and their prey (15 million tonnes) was estimated with an energy budget of the Georges Bank ecosystem (Sissenwine et al., 1984). Results of the MSVPA were insensitive to the assumed level of other food (Tsou and Collie, 21). We performed an eight-species MSVPA of the Georges Bank fish community (Figure 1) for As predators, we included cod (Gadus morhua), silver hake (Merluccius bilinearis), haddock (Melanogrammus aeglefinus), spiny dogfish (Squalus acanthias), and winter skate (Raja ocellata); as prey, cod, silver hake, herring (Clupea harengus), mackerel (Scomber scombrus), and yellowtail flounder (Limanda ferruginea). Spiny dogfish and winter skate were incorporated as other predators, whose abundances were estimated external to the MSVPA from survey data (Tsou and Collie, 21). Inputs are quarterly catch-at-age, terminal Cod Yellowtail flounder Herring Mackerel Figure 1. Partial food web for the Georges Bank fish community as included in the MSVPA (the arrows point from prey to predator species). fishing mortality rates, residual natural mortality rates (.2 for age 1+;.3 for -group), mean body weights, predator-stomach contents, predator consumption rates, and an estimate of the total biomass of the ecosystem. We adopted catch-at-age data and terminal fishing mortalities from single-species stock-assessment documents. As silver hake, herring, and mackerel are assessed over a wider geographic area than Georges Bank, their catches were pro-rated by their average biomass proportions on Georges Bank (.19,.121, and.126, respectively; Collie and DeLong, 1999). Consumption rates by predator age were from previous studies: dogfish from Jones and Geen (1977); cod, silver hake, and haddock from Grosslein et al. (198); and winter skate from Nelson (1993). Diet composition by predator and prey size/age categories is the foundation of MSVPA. Since beginning in 1968, thousands of stomach samples from marine fish have been gathered along the northeast coast of North America and analysed. We extracted stomach-content data from the food-habit database. The stomach-content data for were tuned to the simulated populations in those years to obtain the suitability indices. A prey item was included in the analysis only if it was identified to species level and constituted more than.1% of a predator s diet composition over the sampling period and study area. Predator size was recorded for each stomach; however, only a small fraction of the stomach contents has been classified by size/age class of prey. To circumvent this problem, predator size-preference functions of cod, silver hake, haddock, dogfish, and winter skate were fitted with gamma distributions to distribute the ingested prey into size categories (Tsou and Collie, 21). Distributions by size classes were further converted into age classes based on growth curves. Results on young fish was high compared with fishing mortality and the constant natural mortality rate of.2 that is generally assumed for these stocks (Figure 2). Averaged across years, age and age 1 silver hake experienced the highest predation mortality among the six prey species: approximately 1.1 for age and 1.6 for age 1 silver hake. Cannibalism was the dominant source of predation mortality and accounted, on average, for 7% and 6% of predation mortality on age and age 1 silver hake, respectively. Haddock was another important predator of age silver hake, accounting for 15% of the predation, while cod was responsible for 3% of the predation mortality on age 1. Based on the estimated predator prey size preference function (Tsou and Collie, 21), cod prey heavily on age 1 silver hake, resulting in the higher predation

3 996 T. S. Tsou and J. S. Collie Cod Silver hake Haddock Mackerel Prey species Herring Yellowtail flounder Figure 2. Predation mortalities of age (closed) and age 1 (hatched) prey as estimated from MSVPA, averaged over years. mortality than on age. Predation on age and age 1 cod from the five predators was not high (average.35 and.2, respectively). The most important predator of age cod was silver hake, which accounted for more than 4% of the predation. Cannibalism and dogfish were each responsible for another 3%. Age 1 cod experienced lower predation than age, the dominant source being cannibalism. Haddock experienced high predation at age (1.1) and cod was its main predator. Average predation on young mackerel was low because its abundance increased sharply during the period, predators preferred older mackerel based on our predator size preference functions, and mackerel was infrequently identified to species level in the stomach-content database. Herring was another important prey species that experienced predation mortality of.2 at age and of.7 at age 1. Silver hake was the dominant predator (8% of predation mortality). Predation on age 1 was three times higher than on age because of the difference in preference of silver hake. Yellowtail flounder experienced very low age predation mortality and a predation mortality rate of.2 at age 1. This is because its major predator, dogfish, preferred the size of age 1 yellowtail flounder and age was not selected according to the size-preference function. Although yellowtail flounder constituted a small proportion of the spiny dogfish diet, predation mortality was substantial because dogfish far outnumbered the flounder. When summed over the age groups, the proportion of biomass consumed by predators increased with stock Cod Silver hake Proportion consumed Haddock Mackerel Herring.2 Yellowtail flounder Stock biomass (kt) Figure 3. Relationships between the proportion of biomass consumed and prey biomass as estimated from MSVPA (solid lines: smoothed with super smoother in S-Plus). 25

4 Predation-mediated recruitment in the Georges Bank fish community Age abundance (millions) Age abundance (millions) Age 2 abundance (millions) Figure 4. Silver hake: age 1 vs. age and age 2 vs. age 1 abundance (left panels; broken line: average survival rate) and predation mortality vs. age and age 1 abundance (right panels; solid line: smoothed values) Age abundance (millions) Age abundance (millions) 8 Age 2 abundance (millions) Figure 5. Herring: as in Figure 4. biomass for cod, silver hake, and yellowtail flounder, whereas the proportion declined with increasing stock biomass for haddock, mackerel, and herring (Figure 3). The increasing trends for cod and silver hake might be caused by cannibalism. The decreasing trends for mackerel and herring may indicate predator saturation

5 998 T. S. Tsou and J. S. Collie Age abundance (millions) Age abundance (millions) 12 Age 2 abundance (millions) Figure 6. Cod: as in Figure Age abundance (millions) Age abundance (millions) 5 Age 2 abundance (millions) Figure 7. Haddock: as in Figure 4 (the two largest year classes were excluded from the plot). because the abundance of pelagics has increased sharply since the mid-198s. The MSVPA equations predict that if predator abundance is constant predation rates should decline as a function of prey stock biomass. In the case of cannibalism, predation rates increase with stock biomass because predator abundance is a multiplier.

6 Predation-mediated recruitment in the Georges Bank fish community 999 Predation from cannibalism Predation from cannibalism (a) (b) Stock biomass Figure 8. on age (open circle) and age 1 (closed triangle) resulting from cannibalism for (a) cod and (b) silver hake. Year-class sizes estimated at different ages were substantially modified by age and age 1 predation. Because predation was high for both age and age 1 silver hake, the relationships of age 1 vs. age and age 2 vs. age 1 abundance were scattered along the mean mortality line (Figure 4). The abundant 1979 cohort of age silver hake experienced above average predation and thus did not result in a large cohort at age 1. Conversely, the 1986 year class experienced low predation mortality as 1-group, resulting in the largest cohort at age 2. For herring, the relationship between age 1 and age abundance was almost linear (Figure 5). was somewhat variable, but had only minor effects on relative year-class size. The relationship between age 2 and age 1 herring was more scattered because age 1 experienced predation mortality three times that of age. For cod (Figure 6), the relationships were fairly linear, because predation mortality was about the same as residual mortality. This was also the case for age 1 haddock (Figure 7), but the age 1 vs. age relationship was more scattered because of the high predation mortality on -group. on age and age 1 silver hake appeared to increase with prey abundance (Figure 4). This compensatory mortality would be expected when cannibalism is a significant component of the total predation. Age 1 cod also experienced a high cannibalism rate and exhibited compensatory mortality as well (Figure 6). In contrast, predation mortality on juvenile herring (Figure 5) and juvenile haddock (Figure 7) showed a weak negative relationship with their abundance, suggesting density independent or weakly depensatory predation. Cannibalism was important for cod and silver hake, but to a different extent among years (Figure 8). Cannibalism of cod was high before 1983 and low afterward, except in Cannibalism increased slightly with increasing stock biomass. Rates of cannibalism in silver hake were more variable for age than for age 1, but both showed a clear increasing trend with stock biomass. Discussion The MSVPA results agree with previous conclusions that predation is a dominant source of mortality in the Georges Bank fish community (Sissenwine et al., 1984; Fogarty and Murawski, 1998; Collie and DeLong, 1999). Strong interactions exist between cod and silver hake as predators and silver hake and herring as prey, while weaker trophic interactions exist for haddock, yellowtail flounder, dogfish, and winter skate. A comparison of age 1 recruits estimated from single species VPA and MSVPA (Figure 9) indicates a difference up to one order of magnitude for some prey species. For herring and yellowtail flounder, which experienced most predation at age 1, the relationship was more scattered than for other species. The results obtained are conditioned on the assumptions and input data for MSVPA. Silver hake abundance is uncertain because an analytical stock assessment is lacking. estimates were sensitive to the input values of predator consumption rates and the size-preference functions influenced the distribution of predation among prey age groups (Tsou and Collie, 21). There is also unobserved mortality of fish larvae and juveniles that is not included in the MSVPA owing to their absence from food-habits data. Nevertheless, our results suggest that predation mortality is large and variable enough to affect year-class size of herring and silver hake significantly. Therefore, predation mortality should be accounted for when making medium- and long-term forecasts of recruitment. Acknowledgements We thank Michael Fogarty for his advice on multispecies analysis and Rodney Rountree, Jason Link, and Lance Garrison for their help in accessing the NEFSC food-habits database; Jack Finn provided the original MSVPA FORTRAN program. The study was funded by the NOAA Coastal Ocean Program, Georges Bank Predation Study, NA36RG474.

7 1 T. S. Tsou and J. S. Collie Cod Haddock Herring 5 Yellowtail flounder SSVPA recruits Mackerel SSVPA recruits Figure 9. Comparison between age 1 recruits (millions) estimated from single-species VPA (SSVPA) and MSVPA (extremely high recruitment of mackerel in 1979 and herring in 1983 were excluded from the plot). References Andersen, K. P., and Ursin, E A multispecies extension to the Beverton and Holt theory of fishing; with accounts of phosphorus, circulation and primary production. Meddelelser fra Danmarks Fiskeri- og Havundersgelser. N.S., 7: Bax, N. J A comparison of the fish biomass flow to fish, fisheries, and mammals in six marine ecosystems. ICES Marine Science Symposia, 193:

8 Predation-mediated recruitment in the Georges Bank fish community 11 Collie, J. S., and DeLong, A. K Multispecies interactions in the Georges Bank fish community. Ecosystem approaches for fisheries management, Alaska Sea Grant College Program, AK SG 99 1: Fogarty, M. J., and Murawski, S. A Large-scale disturbance and the structure of marine systems: fisheries impacts on Georges Bank. Ecological Applications, 8: S6 S22. Grosslein, M. D., Langton, R. W., and Sissenwine, M. P Recent fluctuations in pelagic fish stocks of the Northwest Atlantic, Georges Bank region, in relation to species interactions. Rapports et Procès-Verbaux des Réunions du Conseil International pour l Exploration de la Mer, 177: Gulland, J. A Estimation of mortality rates. Annex to Arctic Fisheries Working Group Report. ICES CM 1965: Doc. 3, 9 pp. Jones, B. C., and Geen, G. H Food and feeding of spiny dogfish (Squalus acanthias) in British Columbia waters. Journal of the Fisheries Research Board of Canada, 34: Nelson, G. A The potential impacts of skate abundances upon the invertebrate resources and growth of yellowtail flounder (Pleuronectes ferrugineus) on Georges Bank. Doctoral dissertation, University of Massachusetts. Overholtz, W. J., Murawski, S. A., and Foster, K. L Impact of predatory fish, marine mammals, and seabirds on the pelagic fish ecosystem of the northeastern USA. ICES Marine Science Symposia, 193: Pope, J. G The ICES Multispecies Assessment Working Group: Evolution, Insights, and Future Problems. ICES Marine Science Symposia, 193: Sissenwine, M. P Perturbation of a predator-controlled continental shelf ecosystem. In Variability and Management of Large Marine Ecosystems, pp Ed. by K. Sherman, and L. M. Alexander. American Association for the Advancement of Science, Selected Symposium Series, no. 99. Sissenwine, M. P., Cohen, E. B., and Grosslein, M. D Structure of the Georges Bank ecosystem. Rapports et Procès-Verbaux des Réunions du Conseil International pour l Exploration de la Mer, 183: Sparre, P A goal function of fisheries (Legion Analysis). ICES CM 198/G: 4. Sparre, P Introduction to multispecies virtual population analysis. ICES Marine Science Symposia, 193: Tsou, T. S., and Collie, J. S. 21. Estimating predation in the Georges Bank fish community. Canadian Journal of Fisheries and Aquatic Sciences, 58:

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