Precaution

Precaution applied to the assessment of evidence

  1. As discussed above, the available information from UKCEH on seabird demography from the Isle of May includes the return rate of individually marked birds from one breeding season to the following season. This is used in this report as a proxy for apparent adult survival. The analysis of resighting information of marked birds to estimate survival accounts for birds that were not seen on one breeding season but were seen in a subsequent breeding season. Consequently, the return rate will be a smaller estimate of adult survival rather than the modelled apparent survival. This is therefore a precautionary estimate of adult survival. However, it is likely that the relationship with sandeel TSB in SA4 would have remained very similar had apparent adult survival been used, only with the adult survival data based on slightly larger values across the range of TSB values. In addition, the scenario testing approach examined the effect of change in adult survival between two sandeel TSB values. The change in adult survival would likely have been much the same between return rate data and apparent survival data, so the Population Viability Analysis (PVA) metrics used to assess the effectiveness of the scenarios would have likely been the same, or very similar. This is outlined in Section 1.8 below.
  2. In conclusion, any precaution in using return rate as a proxy for apparent survival would likely have made little or no difference in the assessment of the benefit of the proposed compensation measures.

Impact scenarios

  1. The impact scenarios used in the assessment within this report were identical to those used in the Report to Inform the Appropriate Assessment (RIAA). This provided three impact scenarios based on advice from NatureScot, Marine Scotland Science and a developer preferred approach. While all three impact levels were considered, conclusions on the efficacy of the proposed sandeel fisheries compensatory measures were based on the most precautionary of these three scenarios. The assessment included the other impact scenarios to provide a suitable context for a range of plausible, but still precautionary, predictions of impacts on the qualifying features of the SPAs under consideration.

Compensation scenarios

  1. The approach used to assess the level of benefit predicted to occur from the proposed compensatory measures was based on a scenario testing approach. Scenarios were based on the potential changes in sandeel TSB in SA4 as a result of changes to fisheries management. Five scenarios were chosen that reflected both the range of historic sandeel TSB values in SA4 and the non-linear relationship between sandeel TSB and either survival or productivity.
  2. Five scenarios were examined (see Section 1.8) that covered the distribution of historic sandeel TSB data, with conclusions based on the most precautionary scenario (this was the change in sandeel TSB from 300,000 tonnes to 400,000 tonnes). It is important to note that this was not a prediction of the expected change in sandeel TSB as a result of the compensatory measure, but only a realistic worst-case scenario to help aid decision making. Scenarios were based on changes in TSB of 100,000 tonnes, so that the five scenarios covered the bulk of the historic TSB data and reflected the levels of change seen in TSB across the available dataset.
  3. This most precautionary improvement in seabird demography was then compared with the three impact scenarios, which included the most precautionary impact scenario. Thus, the conclusions were based on the likelihood that a worst-case compensation benefit would be sufficient to overcome a worst case impact prediction. This is a highly precautionary approach, which was chosen to improve the confidence that could be placed in the results.

Confidence

Evidence from other sandeel stocks

  1. The confidence in the effect of changes in sandeel stocks in SA4 on seabird demographics was increased by the presence of evidence from other sandeel stocks in the North Sea. Evidence of the effects of declining sandeel stocks on kittiwake productivity and survival were shown in SA7 (see Figure 1.5   Open ▸ , and Oro and Furness 2002). The hindcast modelling by Lindegren et al. (2018) showed that sandeel stocks in SA1r would be larger with lower fishing mortality. The Ecopath with Ecosim modelling by Natural England (unpublished at the time of writing) also showed that reducing, or closing, the sandeel fishery in the North Sea would result in increases in sandeel stock biomass and increases in the populations of predatory fish, seabird and mammal species that feed on these stocks.
  2. These additional pieces of evidence lend weight to the evidence shown in this report and increases confidence that change in the management of the sandeel stock in SA4 would result in benefits to both the stock itself and a wide variety of species that forage on this stock.

Evidence from other seabird/fisheries interactions

  1. The review of the effectiveness of Marine Protected Areas, and specifically the effects of changes to fish stock protection or exploitation (see Annex A) showed that there are many instances, from a wide variety of fish species, fisheries types and seabird species, from around the world of the benefits of fisheries management practices that take seabird foraging needs into account. Many of these were included in the analysis by Cury et al. (2011), which also included the North Sea sandeel stock. The presence of multiple examples of the positive effects of fisheries management changes to benefit seabirds increases the confidence that the proposed compensatory measures for the Proposed Development will also result in benefits to breeding seabird populations in SA4.

Discussion and Conclusions

  1. The uncertainties in the information used in this report to show the effectiveness of the proposed sandeel fisheries compensatory measures were identified. By identifying these uncertainties it was possible to determine the effect of these on the assessment of the effectiveness of the proposed measures. In several important cases, most notably the use of return rates as a proxy value for adult survival, the presence of uncertainties in the underlying data was unlikely to have had any important effect on assessment of compensation effectiveness.
  2. To manage the uncertainty in both the impact assessment and the assessment of the effectiveness of the proposed sandeel fisheries compensatory measures to overcome these a suitable precautionary approach was applied. This was mainly through the identification of reasonable worst-case impact and compensation scenarios. By comparing the worst case (i.e. highest) impact scenario against the worst case (i.e. lowest) benefit from compensation a highly precautionary approach was taken. By applying this precautionary approach confidence that the proposed compensatory measures will be sufficient is greatly increased.
  3. Confidence was also improved through the building of the evidence from other studies to support the concept of the sandeel fisheries stock management as a compensatory measure. Evidence was shown for the benefits from other fisheries and seabird populations around the world, and from other sandeel stocks in the North Sea.

1.11. General conclusions

  1. There is strong evidence globally that conservation management measures to reduce or eliminate fishing mortality on seabird prey fish stock has had important benefits across a wide variety of fish species, fisheries and seabirds. This led to the conclusion that similar measures on sandeel stocks in the North Sea could be used to positively affect seabird populations predicted to be impacted by the Proposed Development.
  2. It was therefore important to determine if the sandeel stock in the North Sea could be managed to increase the stock of prey for seabirds. There was strong evidence that the sandeel population in the North Sea, including in SA4, was smaller than historic records show and that this was primarily due to high fishing mortality, both in the recent past and currently. There was also strong evidence that in SA4 specific management measures to increase the stock had only been partially effective. The sandeel box has displaced fisheries to the waters outside the box, while simultaneously basing the TAC on the total populations of sandeels in SA4 (including inside the box), resulting in much higher fishing mortality on the remaining sandeels outside the box in SA4.
  3. There is strong evidence that sandeel stocks are important for seabirds foraging in the North Sea during the breeding season. There is strong evidence that kittiwake breeding success and survival are influenced strongly by sandeel abundance. There is also good evidence that sandeel abundance has an influence on the breeding success of other seabirds. There is strong evidence that the foraging range of seabirds varies during the breeding season and that seabirds in SA4 are likely to rely on sandeel abundance across a large part of the area outside the sandeel box.
  4. The presence of strong published evidence that sandeel abundance strongly affected breeding success and abundance across a wide range of breeding seabird species led to analyses to examine if similar relationships occurred for kittiwake, guillemot, razorbill and puffin foraging in SA4. Strong relationships were found between sandeel abundance and seabird abundance, productivity and return rate (a proxy for adult survival) for all the species assessed, except for razorbill, where there was no relationship with productivity.
  5. There was also strong evidence of recovery of sandeel stocks in the North Sea following closure of the fishery. This included evidence from the sandeel box in SA4.
  6. Various elements combined to strongly suggest that SA4 is likely to be the most effective scale for compensation. Foraging range information, based on tracking data from a relatively limited period of the annual cycle, showed that important areas of sandeel habitat occurred outside the box. New analyses of kittiwake productivity from colonies within SA4 that either adjacent to the box or outside the box showed no important difference in the relationship between productivity and TSB in SA4. This finding adds to the evidence that seabird populations are responding to the sandeel population size across the whole of SA4, and that the sandeel box has been only partially successful at mitigating the impacts of the fishery on seabird populations. Finally, the presence of strong relationships between each of adult population size, return rates and productivity and TSB in SA4 showed that the population is responding to changes at this spatial scale. It seems likely, therefore, that this scale is important to seabirds breeding on the Isle of May. This may be because of the importance of areas beyond typical foraging range in poor sandeel years and in the periods of the annual cycle outside the breeding season.
  7. The current management of sandeel stocks in SA4 does not account for the presence of the box. So sandeel TAC is based on the TSB in all of SA4, not just the stock outside the box. Given the sedentary nature of individual sandeels, this suggests that impacts on sandeel stocks outside the box could be particularly severe., These areas may be important to seabirds during periods of the annual cycle not assessed through tracking during the early chick phase.
  8. Thus, reducing or removing fishing pressure across the whole of SA4 is very likely the most effective measure to compensate for predicted impacts. The level of compensation that could potentially be achieved through reducing or removing fishing pressure was then explored.
  9. Likely gains to the SPA populations of kittiwake, guillemot, razorbill, and puffin predicted to be impacted by the proposed development varied across five compensation scenarios. The scenario that produced the smallest benefit to SPA populations was the change in sandeel TSB from 300,000 to 400,000 tonnes. This worst-case benefit to sandeels from reducing or removing fishing pressure was therefore compared with the predicted impacts, including the worst-case impact scenario.
  10. The ability of the proposed compensation measures, reducing or removing fishing pressure in SA4, was tested using relationships between sandeel TSB in SA4 and adult return rate (as a proxy for adult survival) or productivity. The positive effects of predicted changes in demographic parameters were compared with the negative effects of three predicted impact scenarios from the Proposed Development alone.
  11. For all species and all SPAs, it was clear that the predicted minimum benefit from reducing or removing fishing pressure in SA4 was sufficient to compensate for all predicted impact scenarios, including the worst-case scenario.
  12. These analyses have demonstrated that reducing or removing fishing pressure in the remaining area of SA4 outside the sandeel box would provide more than sufficient compensation for the predicted impacts from the Proposed Development. There was sufficient strength in the evidence used to support this assessment, combined with the comparison of a worst-case benefits with worst case predicted impacts, to be sufficiently certain that the proposed sandeel fisheries compensatory measure will ensure the coherence of the UK SPA network.

 

1.12. References and Citations

Abesamis, R.A. and Russ, G.R. 2005. Density-dependent spillover from a marine reserve: long-term evidence. Ecological Applications, 15, 1798-1812.

Adams, N.J., Seddon, P.J., van Heezik, Y.M. 1992. Monitoring of seabirds in the Benguela upwelling system: can seabirds be used as indicators and predictors of change in the marine environment? South African Journal of Marine Science, 12, 959–974.

Alos, J., Puiggros, A., Diaz-Gil, C., Palmer, M., Rossello, R. and Arlinghaus, R. 2015. Empirical evidence for species-specific export of fish naivete from a no-take marine protected area in a coastal recreational hook and line fishery. pLoS ONE, 10, e0135348.

Arias-Del-Razo, A., Schramm, Y., Heckel, G., Saenz-Arroyo, A., Hernandez, A., Vazquez, L. and Carillo-Munoz, A.I. 2019. Do marine reserves increase prey for California sea lions and Pacific harbor seals? pLoS ONE, 14, e0218651.

Arnott, S.A. and Ruxton, G.D. 2002. Sandeel recruitment in the North Sea: demographic, climatic and trophic effects. Marine Ecology Progress Series 238: 199-210.

Auster, P.J., Malatesta, R.J., Langton, R.W., Watting, L., Valentine, P.C., Donaldson, C.L.S., Langton, E.W., Shepard, A.N. and Babb, W.G. 1996. The impacts of mobile fishing gear on seafloor habitats in the Gulf of Maine (Northwest Atlantic): implications for conservation of fish populations. Reviews in Fisheries Science 4: 185-202.

Auster, P.J. and Langton, R.W. 1999. The effects of fishing on fish habitat. Pp. 150-187 in Benaka, L. (Ed.) Fish habitat: essential fish habitat and rehabilitation. American Fisheries Society, Bethesda.

Ballantyne, B. 2014. Fifty years on: lessons from marine reserves in New Zealand and principles for a worldwide network. Biological Conservation, 176, 297-307.

Bedford, J., Ostle, C., Johns, D.G., Atkinson, A., Best, M., Bresnan, E., Machairopoulou, M., Graves, C.A., Devlin, M., Milligan, A., Pitois, S., Mellor, A., Tett, P. and McQuatters-Gollop, A. 2020. Lifeform indicators reveal large-scale shifts in plankton across the north-west European shelf. Global Change Biology 26: 3482-3497.

Behrens, J.W., Aertebjerg, G., Petersen, J.K. and Carstensen, J. 2009. Oxygen deficiency impacts on burying habitats for lesser sandeel, Ammodytes tobianus, in the inner Danish waters. Canadian Journal of Fisheries and Aquatic Sciences 66: 883-895.

Bertrand, S., Joo, R., Smet, C.A., Tremblay, Y., Barbraud, C. and Weimerskirch, H. 2012. Local depletion by a fishery can affect seabird foraging. Journal of Applied Ecology, 49, 1168-1177.

Boersma, P.D., Garcia Borboroglu, P., Gownaris, N.J., Bost, C.A., Chiaradia, A., Ellis, S., Schneider, T., Seddon, P.J., Simeone, A., Trathan, P.N., Waller, L.J. and Wienecke, B. 2020. Applying science to pressing conservation needs for penguins. Conservation Biology, 34, 103-112.

Boulcott, P., Stirling, D., Clarke, J. and Wright, P.J. 2018. Estimating fishery effects in a marine protected area: Lamlash Bay. Aquatic Conservation: Marine and Freshwater Ecosystems, 28, 840-849.

Bradshaw, C., Veale, L.O., Hill, A.S. and Brand, A.R. 2001. The effect of scallop dredging on Irish Sea benthos: experiments using a closed area. Hydrobiologia 465: 129-138.

Bradshaw, C., Veale, L.O. and Brand, A.R. 2002. The role of scallop-dredge disturbance in long-term changes in Irish Sea benthic communities: a re-analysis of an historical dataset. Journal of Sea Research 47: 161-184.

Buxton, C.D. and Smale, M.J. 1989. Abundance and distribution patterns of three temperate marine reef fish (Teleostei: Sparidae) in exploited and unexploited areas off the southern Cape coast. Journal of Applied Ecology, 26, 441-451.

Buxton, C.D., Hartmann, K., Kearney, R. and Gardner, C. 2014. When is spillover from marine reserves likely to benefit fisheries? pLoS ONE, 9, e107032.

Cabral, R.B., Bradley, D., Mayorga, J., Goodell, W., Friedlander, A.M., Sala, E., Costello, C. and Gaines, S.D. 2020. A global network of marine protected areas for food. Proceedings of the National Academy of Sciences of the United States of America, 117, 28134-28139.

Campbell, K.J., Steinfurth, A., Underhill, L.G., Coetzee, J.C., Dyer, B.M., Ludynia, K., Makhado, A.B., Merkle, D., Rademan, J., Upfold, L. and Sherley, R.B. 2019. Local forage fish abundance influences foraging effort and offspring condition in an endangered marine predator. Journal of Applied Ecology, 56, 1751-1760.

Campbell, S.J., Edgar, G.J., Stuart-Smith, R.D., Soler, G. and Bates, A.E. 2018. Fishing-gear restrictions and biomass gains for coral reef fishes in marine protected areas. Conservation Biology, 32, 401-410.

Camphusen, C.J. 2002. Post-fledging dispersal of Common Guillemots Uria aalge guarding chicks in the North Sea: The effect of predator presence and prey availability at sea. Ardea 90: 103-119.

Cappell, R., Robinson, M., Gascoigne, J. and Nimmo, F. 2013. A review of the Scottish scallop fishery. Poseidon report to Marine Scotland. Poseidon Aquatic Resource Management Ltd., Hampshire.

Cappell, R., Huntington, T., Nimmo, F. and MacNab, S. 2018. The UK scallop fishery: current trends, future management options and recommendations. Poseidon report to South West Fish Producer Organisation Ltd. Report Ref. 1417-GBR. Poseidon Aquatic Resource Management Ltd., Hampshire.

Carroll, M.J., Bolton, M., Owen, E., Anderson, G.Q.A., Mackley, E.K., Dunn, E.K. and Furness, R.W. 2017. Kittiwake breeding success in the southern North Sea correlates with prior sandeel fishing mortality. Aquatic Conservation: Marine and Freshwater Ecosystems, 27, 1164-1175.

Chen, W., Staneva, J., Grayek, S., Schulz-Stellenfleth, J. and Greinert, J. 2022. The role of heat wave events in the occurrence and persistence of thermal stratification in the southern North Sea. Natural Hazards and Earth System Science 22: 1683-1698.

Cheung, W.W.L. and Pauly, D. 2016. Impacts and effects of ocean warming on marine fishes. pp. 239-253. In Laffoley, D. and Baxter, J.M. (eds.) Explaining ocean warming: causes, scale, effects and consequences. IUCN, Gland.

Church, N.J., Carter, A.J., Tobin, D., Edwards, D., Eassom, A., Cameron, A., Johnson, G.E., Robson, L.M. and Webb, K.E. 2016. JNCC Pressure Mapping Methodology Physical Damage (Reversible Change) – Penetration and/or disturbance of the substrate below the surface of the seabed, including abrasion. JNCC Report No. 515. JNCC, Peterborough.

Clairbaux, M., Cheung, W.W.L., Mathewson, P., Porter, W., Courbin, N., Fort, J., Strøm, H., Moe, B., Fauchald, P. et al. 2021. Meeting Paris agreement objectives will temper seabird winter distribution shifts in the North Atlantic Ocean. Global Change Biology, doi: 10.1111/gcb.15497.

Cleasby, I.R., Owen, E., Wilson, L., Wakefield, E.D., O’Connell, P. and Bolton, M. 2020. Identifying important at-sea areas for seabirds using species distribution models and hotspot mapping. Biological Conservation, 241, 108375.

Cohen, P.J. and Alexander, T.J. 2013. Catch rates, composition and fish size from reefs managed with periodically-harvested closures. pLoS ONE, 8, e73383.

Collie, J.S. and Escanero, G.A. 2000. Photographic evaluation of the impacts of bottom fishing on benthic epifauna. ICES Journal of Marine Science 57: 987-1001.

Collie, J.S., Escanero, G.A. and Valentine, P.C. 1997. Effects of bottom fishing on the benthic megafauna of Georges Bank. Marine Ecology Progress Series 155: 159-172.

Coulson, J.C. and Coulson, B.A., 2008. Measuring immigration and philopatry in seabirds; recruitment to Black‐legged Kittiwake colonies. Ibis, 150: 288-299.

Cowley, P.D., Brouwer, S.L. and Tilney, R.L. 2002. The role of the Tsitsikamma National Park in the management of four shore-angling fish along the south-eastern Cape coast of South Africa. South African Journal of Marine Science, 24, 27-35.

Crawford, R.J.M. 1998. Responses of African penguins to regime changes of sardine and anchovy in the Benguela system. South African Journal of Marine Science, 19, 355–364.

Crawford, R.J.M., Shannon, L.J., Whittington, P.A. 1999. Population dynamics of the African penguin Spheniscus demersus at Robben Island, South Africa. Marine Ornithology, 27, 139–147.

Crawford, R.J.M., Barham, P.J., Underhill, L.G., Shannon, L.J., Coetzee, J.C., Dyer, B.M., Leshoro, T.M. and Upfold, L. 2006. The influence of food availability on breeding success of African penguins Spheniscus demersus at Robben Island, South Africa. Biological Conservation, 132, 119-125. 

Crawford, R.J.M., Sydeman, W.J., Thompson, S.A., Sherley, R.B. and Makhado, A.B. 2019. Food habits of an endangered seabird indicate recent poor forage fish availability off western South Africa. ICES Journal of Marine Science, 76, 1344-1352.

Critchley, E.J., Grecian, W.J., Bennison, A., Kane, A., Wischnewski, S., Canadas, A., Tierney, D., Quinn, J.L. and Jessopp, M.J. 2019. Assessing the effectiveness of foraging radius models for seabird distributions using biotelemetry and survey data. Ecography, 43, 184-196.

Cury, P.M., Boyd, I.L., Bonhommeau, S., Anker-Nilssen, T., Crawford, R.J.M., Furness, R.W., Mills, J.A., Murphy, E.J., Österblom, H., Paleczny, M., Piatt, J.F., Roux, J-P., Shannon, L. and Sydeman, W.J. 2011.  Global seabird response to forage fish depletion – one-third for the birds.  Science, 334, 1703-1706.

Dahood, A., de Mutsert, K. and Watters, G.M. 2020. Evaluating Antarctic marine protected area scenarios using a dynamic food web model. Biological Conservation, 251, 108766.

Daunt, F., Fang, Z., Howells, R., Harris, M., Wanless, S., Searle, K. and Elston, D. 2020. Improving estimates of seabird body mass survival relationships. Scottish Marine and Freshwater Science 11: 13, DOI: 10.7489/12329-1

Daunt, F., Wanless, S., Greenstreet, S. P. R., Jensen, H., Hamer, K. C., and Harris, M. P. 2008. The impact of the sandeel fishery closure on seabird food consumption, distribution, and productivity in the northwestern North Sea. Canadian Journal of Fisheries and Aquatic Sciences, 65, 362-381.

Davis, S.E., Nager, R.G. and Furness, R.W. 2005. Food availability affects adult survival as well as breeding success of parasitic jaegers. Ecology, 86, 1047-1056.

Dayton, P.K., Thrush, S.F., Agardy, M.T. and Hofman, R.J. 1995. Environmental effects of marine fishing. Aquatic Conservation: Marine and Freshwater Ecosystems 5: 205-232.

Di Lorenzo, M., Claudet, J. and Guidetti, P. 2016. Spillover from marine protected areas to adjacent fisheries has an ecological and a fishery component. Journal for Nature Conservation, 32, 62-66.

Di Lorenzo, M., Guidetti, P., Franco, A., Calo, A. and Claudet, J. 2020. Assessing spillover from marine protected areas and its drivers: a meta-analytical approach. Fish and Fisheries, 21, 906-915.

DTA Ecology. 2021. Framework to evaluate ornithological compensatory measures for offshore wind: process guidance note for developers. Advice to Marine Scotland. Doc. Ref. 1107 Marine Scotland CM framework.

Dunn, E. 2021. Revive our Seas: The case for stronger regulation of sandeel fisheries in UK waters. RSPB, Sandy

Edgar, G.J., Stuart-Smith, R.D., Willis, T.J., Kininmonth, S., Baker, S.C., Banks, S., Barrett, N.S., Becerro, M.A., Bernard, A.T.F., Berkhout, J., Buxton, C.D., Campbell, S. J., Cooper, A.T., Davey, M., Edgar, S.C. et al. 2014. Global conservation outcomes depend on marine protected areas with five key features. Nature, 506, 216–220.

Eleftheriou, A. and Robertson, M.R. 1992. The effects of experimental scallop dredging on the fauna and physical environment of a shallow sandy community. Netherlands Journal of Sea Research 30: 289-299.

Elliott, K.H., Woo, K.J., Gaston, A.J., Benvenuti, S., Dall'Antonia, L. and Davoren, G.K., 2009. Central-place foraging in an Arctic seabird provides evidence for Storer-Ashmole's halo. The Auk, 126: 613-625.

Enever, R., Doherty, P.D., Ashworth, J., Duffy, M., Kibel, P., Parker, M., Stewart, B.D. and Godley, B.J., 2022. Scallop potting with lights: A novel, low impact method for catching European king scallop (Pecten maximus). Fisheries Research, 252 https://doi.org/10.1016/j.fishres.2022.106334.

Engelhard, G.H., Peck, M.A., Rindorf, A., Smout, S.C., van Deurs, M., Raab, K., Andersen, K.H., Garthe, S., Lauerburg, R.A.M., Scott, F., Brunel, T., Aarts, G., van Kooten, T. and Dickey-Collas, M. 2014. Forage fish, their fisheries, and their predators: who drives whom? ICES Journal of Marine Science, 71, 90-104.

European Commission. 2012. Guidance document on Article 6(4) of the 'Habitats Directive' 92/43/EEC: clarification of the concepts of: alternative solutions, imperative reasons of overriding public interest, compensatory measures, overall coherence, opinion of the commission. https://ec.europa.eu/environment/nature/natura2000/management/docs/art6/new_guidance_art6_4_en.pdf

Fayet, A.L., Clucas, G.V., Anker‐Nilssen, T., Syposz, M. and Hansen, E.S., 2021. Local prey shortages drive foraging costs and breeding success in a declining seabird, the Atlantic puffin. Journal of Animal Ecology 90:1152-1164.

Fernandez-Chacon, A., Villegas-Rios, D., Moland, E., Baskett, M.L., Olsen, E.M. and Carlson, S.M. 2020. Protected areas buffer against harvest selection and rebuild phenotypic complexity. Ecological Applications, 30, e02108.

Florin, A.B., Bergström, U., Ustups, D., Lundström, K. and Jonsson, P.R. 2013. Effects of a large northern European no-take zone on flatfish populations. Journal of Fish Biology, 83, 939–962.

Frederiksen, M., Wanless, S., Harris, M.P., Rothery, P. and Wilson, L.J. 2004. The role of industrial fisheries and oceanographic change in the decline of North Sea black-legged kittiwakes. Journal of Applied Ecology, 41, 1129-1139.

Frederiksen, M., Wright, P.J., Harris, M.P., Mavor, R.A., Heubeck, M. & Wanless, S. 2005. Regional patterns of kittiwake Rissa tridactyla breeding success are related to variability in sandeel recruitment. Marine Ecology Progress Series, 300, 201-211.

Frederiksen, M., Edwards, M., Richardson, A. J., Halliday, N. C., and Wanless, S. 2006. From plankton to top predators: bottom-up control of a marine food web across four trophic levels. Journal of Animal Ecology, 75, 1259-1268.

Frederiksen, M., Edwards, M., Mavor, R. A., and Wanless, S. 2007b. Regional and annual variation in black-legged kittiwake breeding productivity is related to sea surface temperature. Marine Ecology Progress Series, 350, 137-143.

Frederiksen, M., Furness, R.W. and Wanless, S. 2007a. Regional variation in the role of bottom-up and top-down processes in controlling sandeel abundance in the North Sea. Marine Ecology Progress Series, 337, 279-286.

Frederiksen, M., Daunt, F., Harris, M.P. and Wanless, S. 2008a. The demographic impact of extreme events: stochastic weather drives survival and population dynamics in a long-lived seabird. Journal of Animal Ecology, 77, 1020-1029.

Frederiksen, M., Jensen, H., Duant, F., Mavor, R.A. and Wanless, S. 2008b. Differential effects of a local industrial sand lance fishery on seabird breeding performance. Ecological Applications, 18, 701–710.

Funakoshi, S. 1998. Studies on the mechanisms behind the species replacement between sardine and anchovy populations and the ecology of sandeel for the management of fishery resources. Bulletin of the Japanese Society of Fisheries Oceanography 62: 218-234.

Furness, R.W. 2007. Responses of seabirds to depletion of food fish stocks. Journal of Ornithology, 148, 247–252.

Furness, R.W. and Tasker, M.L. 2000. Seabird-fishery interactions: quantifying the sensitivity of seabirds to reductions in sandeel abundance, and identification of key areas for sensitive seabirds in the North Sea. Marine Ecology Progress Series, 202, 253–264.

Gao, S., Hjøllo, S.S., Falkenhaug, T., Strand, E., Edwards, M. and Skogen, M.D. 2021. Overwintering distribution, inflow patterns and sustainability of Calanus finmarchicus in the North Sea. Progress in Oceanography 194: 102567.

Garcia-Rubies, A., Hereu, B. and Zabala, M. 2013. Long-term recovery patterns and limited spillover of large predatory fish in a Mediterranean MPA. pLoS ONE, 8, e73922.

Gaspar, C., Giménez, J., Andonegi, E., Astarloa, A., Chouvelon, T., Franco, J., Goñi, N., Corrales, X., Spitz, J., Bustamente, P. and Louzao, M. 2022. Trophic ecology of northern gannets Morus bassanus highlights the extent of isotopic niche overlap with other apex predators within the Bay of Biscay. Marine Biology 169: 105.

Gell, F.R. and Roberts, C.M. 2003. Benefits beyond boundaries: the fishery effects of marine reserves. Trends in Ecology and Evolution, 18, 448-455.

Giakoumi, S., McGowan, J., Mills, M., Beger, M., Bustamante, R.H., Charles, A., Christie, P., Fox, M., Garcia-Borboroglu, P., Gelcich, S., Guidetti, P., Mackelworth, P., Maina, J.M., McCook, L., Micheli, F., Morgan, L.E., Mumby, P.J., Reyes, L.M., White, A., Grorud-Colvert, K. and Possingham, H.P. 2018. Revisiting “success” and “failure” of marine protected areas: A conservation scientist perspective. Frontiers in Marine Science, 5, 223.

Goni, R., Adlerstein, S., Alvarez-Berastegui, D., Forcada, A., Renones, O., Criquet, G., Polti, S., Cadiou, G., Valle, C., Lenfant, P., Bonhomme, P., Perez-Ruzafa, A., Sanchez-Lizaso, J.L., Garcia-Charton, J.A., Bernard, G., Stelzenmuller, V. and Planes, S. 2008. Spillover from six western Mediterranean marine protected areas: evidence from artisanal fisheries. Marine Ecology Progress Series, 366, 159-174.

Goni, R., Hilborn, R., Diaz, D., Mallol, S. and Adlerstein, S. 2010. Net contribution of spillover from a marine reserve to fishery catches. Marine Ecology Progress Series, 400, 233-243.

Greenstreet, S., Fraser, H., Armstrong, E. and Gibb, I. 2010. Monitoring the consequences of the northwestern North Sea sandeel fishery closure. Scottish Marine and Freshwater Science, 1, 1–31.

Hall-Spencer, J.M. and Moore, P.G. 2000. Impact of scallop dredging on maerl grounds. P 10-5-118 in Kaiser, M.J. and De Groot, S.J. (Eds). Effects of fishing on non-target species and habitats: biological, conservation and socio-economic issues. Blackwell, Oxford.

Halouani, G., Villanueva, C.M., Raoux, A., Dauvin, J.C., Lasram, F.B., Foucher, E., Le Loc’h, F., Safi, G., Araignous, E., Robin, J.P. and Niquil, N. 2020. A spatial food web model to investigate potential spillover effects of a fishery closure in an offshore wind farm. Journal of Marine Systems, 212, 103434.

Handley, J.M., Pearmain, E.J., Oppel, S., Carneiro, A.P.B., Hazin, C., Phillips, R.A. et al. 2020. Evaluating the effectiveness of a large multi-use MPA in protecting key biodiversity areas for marine predators. Diversity and Distributions, 26, 715-729.

Harmelin-Vivien, M., Le Direach, L., Bayle-Sempere, J., Charbonnel, E., Garcia-Charton, J.A., Ody, D., Perez-Ruzafa, A., Renones, O., Sanchez-Jerez, P. and Valle, C. 2008. Gradients of abundance and biomass across reserve boundaries in six Mediterranean marine protected areas: evidence of fish spillover? Biological Conservation, 141, 1829-1839.

Harris, M.P., Bogdanova, M.I., Daunt, F. and Wanless, S., 2012. Using GPS technology to assess feeding areas of Atlantic Puffins Fratercula arctica. Ringing & Migration 27:43-49.

Hays, G.C., Koldewey, H.J., Andrzejaczek, S., Attrill, M.J., Barley, S., Bayley, D.T.I., Benkwitt, C.E., Block, B., Schallert, R.J., Carlisle, A.B. et al. 2020. A review of a decade of lessons from one of the world’s largest MPAs: conservation gains and key challenges. Marine Biology, 167, 159.

Heerah, K., Dias, M.P., Delord, K., Oppel, S., Barbraud, C., Weimerskirch, H. and Bost, C.A. 2019. Important areas and conservation sites for a community of globally threatened marine predators of the southern Indian Ocean. Biological Conservation, 234, 192-201.

Heessen, H.J.L., Daan, N. and Ellis, J.R. 2015. Fish Atlas of the Celtic Sea, North Sea, and Baltic Sea. KNNV Publishing, The Netherlands.

Henriksen, O., Christensen, A., Jonasdottir, S., MacKenzie, B.R., Nielsen, K.E., Mosegaard, H. and van Deurs, M. 2018. Oceanographic flow regime and fish recruitment: reversed circulation in the North Sea coincides with unusually strong sandeel recruitment. Marine Ecology Progress Series 607: 187-205.

Henriksen, O., Rindorf, A., Brooks, M.E., Lindegren, M. and van Deurs, M. 2021a. Temperature and body size affect recruitment and survival of sandeel across the North Sea. ICES Journal of Marine Science 78: 1409-1420.

Henriksen, O., Rindorf, A., Mosegaard, H. and van Deurs, M. 2021b. Get up early: Revealing behavioral responses of sandeel to ocean warming using commercial catch data. Ecology and Evolution 11: 16786-16805.

Hentati-Sundberg, J., Olin, A.B., Evans, T.J., Isaksson, N., Berglund, P-A. and Olsson, O. 2020. A mechanistic framework to inform the spatial management of conflicting fisheries and top predators. Journal of Applied Ecology, 10.1111/1365-2664.13759

Hill, S.L., Hinke, J., Bertrand, S., Fritz, L., Furness, R.W., Ianelli, J.N., Murphy, M., Oliveros-Ramos, R., Pichegru, L., Sharp, R., Stillman, R.A., Wright, P.J. and Ratcliffe, N. 2020. Reference points for predators will progress ecosystem-based management of fisheries. Fish and Fisheries, 21, 368-378.

Hoskin, M. G., Coleman, R. A., von Carlshausen, E. and Davis, C. M. 2011. Variable population responses by large decapod crustaceans to the establishment of a temperate marine no‐take zone. Canadian Journal of Fisheries and Aquatic Sciences, 68, 185–200.

Howarth, L.M., Wood, H.L., Turner, A.P. and Beukers-Stewart, B.D. 2011. Complex habitat boosts scallop recruitment in a fully protected marine reserve. Marine Biology, 158, 1767-1780.

Howarth, L.M. and Stewart, B.D. 2014. The dredge fishery for scallops in the United Kingdom (UK): effects on marine ecosystems and proposals for future management. Marine Ecosystem Management Report No. 5. University of York, York.s.whiterose.ac.uk/79233/

Huserbråten, M.B.O., Moland, E., Knutsen, H., Olsen, E.M., Andre, C. and Stenseth, N.C. 2013. Conservation, spillover and gene flow within a network of northern European marine protected areas. pLoS ONE, 8, e73388.

ICES. 2021. ICES Advice on fishing opportunities, catch, and effort. Greater North Sea ecoregion: Sandeel (Ammodytes spp.) in divisions 4.a–b, Sandeel Area 4 (northern and central North Sea). https://www.ices.dk/sites/pub/Publication%20Reports/Advice/2021/2021/san.sa.4.pdf  

ICES. 2021b. Working Group on Multispecies Assessment Methods (WGSAM; outputs from 2020 meeting). ICES Scientific Reports. 3:10. 231 pp. https://doi.org/10.17895/ices.pub.7695

ICES. 2022. Herring Assessment Working Group for the area south of 62oN (HAWG). 4:16.

ICES 2017. OSPAR request on the production of spatial layers of fishing intensity/pressure. ICES Technical Service sr.2017.17 (Version 2: 22 January 2019) https://doi.org/10.17895/ices.advice.4683

ICES 2017b. Report of the Benchmark on Sandeel (WKSand 2016), 31 October – 4 November 2016, Bergen, Norway. ICES CM 2016/ACOM:33.

Ito, M., Takahashi, A., Kokubun, N., Kitaysky, A.S. and Watanuki, Y., 2010. Foraging behavior of incubating and chick-rearing thick-billed murres Uria lomvia. Aquatic Biology 8: 279-287.

Jaco, E.M. and Steele, M.A. 2019. Pre-closure fishing pressure predicts effects of marine protected areas. Journal of Applied Ecology, 57, 229-240.

Jennings, S. and Kaiser, M.J. 1998. The effects of fishing on marine ecosystems. Advances in Marine Biology 34: 201-352.

JNCC 2020. Statements on conservation benefits, condition and conservation measures for Firth of Forth Banks complex nature conservation MPA. https://jncc.gov.uk

Jouventin, P., Capdeville, D., Cuenot-Chaillet, F. and Boiteau, C. 1994. Exploitation of pelagic resources by a non-flying seabird: satellite tracking of the king penguin throughout the breeding cycle. Marine Ecology Progress Series 106: 11-19.

Kaiser, M.J., Hill, A.S., Ramsay, K., Spencer, B.E., Brand, A.R., Veale, L.O., Prudden, K., Rees, E.I.S., Munday, B.W., Ball, B. and Hawkins, S.J. 1996. Benthic disturbance by fishing gear in the Irish Sea: a comparison of beam trawling and scallop dredging. Aquatic Conservation: Marine and Freshwater Ecosystems 6: 269-285.

Kelaher, B.P., Tan, M., Figueira, W.F., Gillanders, B.M., Connell, S.D., Goldsworthy, S.D., Hardy, N. and Coleman, M.A. 2015. Fur seal activity moderates the effects of an Australian marine sanctuary on temperate reef fish. Biological Conservation, 182, 205-214.

Kerwath, S.E., Winkler, H., Götz, A. and Attwood, C.G. 2013. Marine protected area improves yield without disadvantaging fishers. Nature Communications, 4, 2347.

Kirkman, S.P., Yemane, D.G., Lamont, T., Meyer, M.A. and Pistorius, P.A. 2016. Foraging behavior of Subantarctic fur seals supports efficiency of a marine reserve’s design. pLoS ONE, 11, e0152370.

Kleiven, P.J.N., Espeland, S.H., Olsen, E.M., Abesamis, R.A., Moland, E. and Kleiven, A.R. 2019. Fishing pressure impacts the abundance gradient of European lobsters across the borders of a newly established marine protected area. Proceedings of the Royal Society B, 286, 20182455.

Kough, A.S., Belak, C.A., Paris, C.B., Lundy, A., Cronin, H., Gnanalingham, G., Hagedorn, S., Skubel, R., Weiler, A.C. and Stoner, A.W. 2019. Ecological spillover from a marine protected area replenishes over-exploited population across an island chain. Conservation Science and Practice, 1, e17.

Laffoley, D. and Baxter, J.M. (eds.) Explaining ocean warming: causes, scale, effects and consequences. IUCN, Gland.

Lambert, G.I., Murray, L.G., Hiddink, J.G., Hinz, H., Lincoln, H., Hold, N., Cambie, G. and Kaiser, M.J. 2017. Defining thresholds of sustainable impact on benthic communities in relation to fishing disturbance. Scientific Reports 7: 5440.

Lane, J.V., Jeavons, R., Deakin, Z., Sherley, R.B., Pollock, C.J., Wanless, R.J. and Hamer, K.C. 2020. Vulnerability of northern gannets to offshore wind farms; seasonal and sex-specific collision risk and demographic consequences. Marine Environmental Research 162: 105196.

Langton, R.W. and Robinson, W.E. 1990. Faunal associations on scallop grounds in the western Gulf of Maine. Journal of Experimental Marine Biology and Ecology 144: 157-171.

Langton, R., Boulcott, P. and Wright, P. 2021. A verified distribution model for the lesser sandeel Ammodytes marinus. Marine Ecology Progress Series 667: 145-159.

Lascelles, B.G., Langham, G.M., Ronconi, R.A. and Reid, J.B. 2012. From hotspots to site protection: identifying marine protected areas for seabirds around the globe. Biological Conservation, 156, 5-14.

Lavers, J.L., Jones, I.L. and Diamond, A.W., 2007. Natal and breeding dispersal of Razorbills (Alca torda) in eastern North America. Waterbirds: 588-594.

LeBlanc, S.N., Benoit, H.P. and Hunt, H.L. 2015. Broad-scale abundance changes are more prevalent than acute fishing impacts in an experimental study of scallop dredging intensity. Fisheries Research 161: 8-20.

Lindegren, M., van Deurs, M., MacKenzie, B.R., Clausen, L.W., Christensen, A. and Rindorf, A. 2018. Productivity and recovery of forage fish under climate change and fishing: North Sea sandeel as a case study. Fisheries Oceanography, 27, 212-221.

Lombard, A.T., Durbach, I., Harris, J.M., Mann-Lang, J., Mann, B.Q., Branch, G.M. and Attwood, C.G. 2020. South Africa’s Tsitsikamma marine protected area – winners and losers. pp. 237-270 in Humphreys, J. and Clark, R.W.E. (eds.) Marine Protected Areas: Science, Policy and Management. Elsevier, Oxford.

Ludynia, K., Kemper, J. and Roux, J-P. 2012. The Namibian islands’ marine protected area: using seabird tracking data to define boundaries and assess their adequacy. Biological Conservation, 156, 136-145.

Ludynia, K., Waller, L.J., Sherley, R.B., Abadi, F., Galada, Y., Geldenhuys, D., Crawford, R.J.M., Shannon, L.J. and Jarre, A. 2014. Processes influencing the population dynamics and conservation of African penguins on Dyer Island, South Africa. African Journal of Marine Science, 36, 253-267.

MacDonald, A., Speirs, D.C., Greenstreet, S.P.R., Boulcott, P. and Heath, M.R. 2019. Trends in sandeel growth and abundance off the east coast of Scotland. Frontiers in Marine Science 6: 201.

MacNeil, M.A., Graham, N.A.J., Cinner, J.E., Wilson, S.K., Williams, I.D., Maina, J., Newman, S., Friedlander, A.M., Jupiter, S., Polunin, N.V.C. and McClanahan, T.R. 2015. Recovery potential of the world’s coral reef fishes. Nature, 520, 341-344.

McClanahan, T.R. and Mangi, S. 2000. Spillover of exploitable fishes from a marine park and its effect on the adjacent fishery. Ecological Applications, 10, 1792-1805.

McClanahan, T.R., Graham, N.A.J., MacNeil, M.A. and Cinner, J.E. 2014. Biomass-based targets and the management of multispecies coral reef fisheries. Conservation Biology, 29, 409-417.

McInnes, A.M., Ryan, P.G., Lacerda, M., Deshaves, J., Goschen, W.S. and Pichegru, L. 2017. Small pelagic fish responses to fine-scale oceanographic conditions: implications for the endangered African penguin. Marine Ecology Progress Series, 569, 187-203.

McInnes, A.M., Ryan, P.G., Lacerda, M. and Pichegru, L. 2019. Targeted prey fields determine foraging effort thresholds of a marine diver: important cues for the sustainable management of fisheries. Journal of Applied Ecology, 56, 2206-2215.

Malcolm, H.A., Williams, J., Schultz, A.L., Neilson, J., Johnstone, N., Knott, N.A., Harasti, D., Coleman, M.A. and Jordan, A. 2018. Targeted fishes are larger and more abundant in ‘no-take’ areas in a subtropical marine park. Estuarine, Coastal and Shelf Science, 212, 118-127.

Marine Scotland 2019. Sandeels (Ammodytes marinus and A. tobianus). Draft Advice Scottish MPAs and fisheries. Version 1.4. Marine Scotland, Edinburgh.

Marine Scotland 2016. Scottish Sea Fisheries Employment 2015. Marine Scotland, Edinburgh.

Marshall, D.J., Gaines, S., Warner, R., Barneche, D.R. and Bode, M. 2019. Underestimating the benefits of marine protected areas for the replenishment of fished populations. Frontiers in Ecology and Environment, 17, 407-413.

Murawski, S.A. 2010. Rebuilding depleted fish stocks: the good, the bad, and, mostly, the ugly. ICES Journal of Marine Science 67: 1830-1840.

NOAA (National Oceanic and Atmospheric Administration). 2021. NOAA Merged Land Ocean Global Surface Temperature Analysis (NOAAGlobalTemp). https://www.ncei.noaa.gov/products/land-based-station/noaa-global-temp

O’Brien, S.H., Webb, A., Brewer, M.J. and Reid, J.B. 2012. Use of kernel density estimation and maximum curvature to set marine protected area boundaries: identifying a Special Protection Area for wintering red-throated divers in the UK. Biological Conservation, 156, 15-21.

O’Leary, B.C., Brown, R.L., Johnson, D.E., von Nordheim, H., Ardron, J., Packeiser, T. and Roberts, C.M. 2012. The first network of marine protected areas (MPAs) in the high seas: the process, the challenges and where next. Marine Policy, 36, 598-605.

O’Neill, F.G., Robertson, M., Summerbell, K., Breen, M. and Robinson, L.A. 2013. The mobilisation of sediment and benthic infauna by scallop dredges. Marine Environmental Research 90: 104-112.

Olin, A.B., Banas, N.S., Johns, D.G., Heath, M.R., Wright, P.J. and Nager, R.G. 2022. Spatio-temporal variation in the zooplankton prey of lesser Sandeels: species and community trait patterns from the continuous plankton recorder. ICES Journal of Marine Science 79: 1649-1661.

Olin, A.B., Banas, N.S., Wright, P.J., Heath, M.R. and Nager, R.G. 2020. Spatial synchrony of breeding success in the black-legged kittiwake Rissa tridactyla reflects the spatial dynamics of its sandeel prey. Marine Ecology Progress Series, 638, 177-190.

Oppel, S., Bolton, M., Carneiro, A.P., Dias, M.P., Green, J.A., Masello, J.F., Phillips, R.A., Owen, E., Quillfeldt, P., Beard, A. and Bertrand, S., 2018. Spatial scales of marine conservation management for breeding seabirds. Marine Policy 98: 37-46.

Oro, D. and Furness, R.W. 2002. Influences of food availability and predation on survival of kittiwakes. Ecology, 83, 2516-2528.

Osborne, O.E., Hara, P.D., Whelan, S., Zandbergen, P., Hatch, S.A. and Elliott, K.H. 2020. Breeding seabirds increase foraging range in response to an extreme marine heatwave. Marine Ecology Progress Series, 646: 161-173.

Parsons, D.M., Babcock, R.C., Hankin, R.K.S., Willis, T.J., Aitken, J.P., O’Dor, R.K. and Jackson, G.D. 2003. Snapper Pagrus auratus (Sparidae) home range dynamics: acoustic tagging studies in a marine reserve. Marine Ecology Progress Series, 262, 253-265.

Parsons, D.M., Shears, N.T., Babcock, R.C. and Haggitt, T.R. 2004. Fine-scale habitat change in a marine reserve, mapped using radio-acoustically positioned video transects. Marine and Freshwater Research, 55, 257-265.

Peron, C., Gremillet, D., Prudor, A., Pettex, E., Saraux, C., Soriano-Redondo, A., Authier, M. and Fort, J. 2013. Importance of coastal marine protected areas for the conservation of pelagic seabirds: the case of vulnerable yelkouan shearwaters in the Mediterranean Sea. Biological Conservation, 168, 210-221.

Perrow, M.R., Harwood, A.J.P., Skeate, E.R., Praca, E. and Eglington, S.M. 2015. Use of multiple data sources and analytical approaches to derive a marine protected area for a breeding seabird. Biological Conservation, 191, 729-738.

Petitgas, P., Alheit, J., Peck, A., Raab, K.E., Irijoien, X., Huret, J., van Kooij, J., Pohlmann, T., Wagner, C., Zarraonaindia, I. and Dickey-Collas, M. 2012. Anchovy population expansion in the North Sea. Marine Ecology Progress Series 444: 1-13.

Pichegru, L., Gremillet, D., Crawford, R.J.M. and Ryan, P.G. 2010. Marine no-take zone rapidly benefits endangered penguin. Biology Letters, 6, 498-501.

Pichegru, L., Ryan, P.G., van Eeden, R., Reid, T., Gremillet, D. and Wanless, R. 2012. Industrial fishing, no-take zones and endangered penguins. Biological Conservation, 156, 117-125.

Raab, K.E. 2013. The European anchovy (Engraulis encrasicolus) increase in the North Sea. PhD thesis, Wageningen University.

Regnier, T., Gibb, F.M. and Wright, P.J. 2017. Importance of trophic mismatch in a winter-hatching species: evidence from lesser sandeel. Marine Ecology Progress Series 567: 185-197.

Regnier, T., Gibb, F.M. and Wright, P.J. 2018. Temperature effects on egg development and larval condition in the lesser sandeel, Ammodytes marinus. Journal of Sea Research 134: 34-41.

Regnier, T., Gibb, F.M. and Wright, P.J. 2019. Understanding temperature effects on recruitment in the context of trophic mismatch. Scientific Reports 9: 15179.

Requena, S., Oppel, S., Bond, A.L., Hall, J., Cleeland, J., Crawford, R.J.M., Davies, D., Dilley, B.J., Glass, T., Makhado, A., Ratcliffe, N., Reid, T.A., Ronconi, R.A., Schofield, A., Steinfurth, A., Wege, M., Bester, M. and Ryan, P.G. 2020. Marine hotspots of activity inform protection of a threatened community of pelagic species in a large oceanic jurisdiction. Animal Conservation, 23, 585-596.

Rindorf, A., Wanless, S. and Harris, M.P., 2000. Effects of changes in sandeel availability on the reproductive output of seabirds. Marine Ecology Progress Series 202: 241-252.

Robertson, G.S., Bolton, M., Grecian, W.J. and Monaghan, P. 2014. Inter-and intra-year variation in foraging areas of breeding kittiwakes (Rissa tridactyla). Marine Biology, 161: 1973-1986.

Robinson, W.M.L., Butterworth, D.S. and Plaganvi, E.E. 2015. Quantifying the projected impact of the South African sardine fishery on the Robben Island penguin colony. ICES Journal of Marine Science, 72, 1822-1833.

Ronconi, R.A., Lascelles, B.G., Longham, G.M., Reid, J.B. and Oro, D. 2012. The role of seabirds in marine protected area identification, delineation, and monitoring: introduction and synthesis. Biological Conservation, 156, 1-4.

Rossiter, J.S. and Levine, A. 2014. What makes a “successful” marine protected area? The unique context of Hawaii’s fish replenishment areas. Marine Policy, 44, 196-203.

Russ, G.R. and Alcala, A.C. 1999. Management histories of Sumilon and Apo Marine Reserves, Philippines, and their influence on national marine resource policy. Coral Reefs, 18, 307-319.

Sackett, D.K., Kelley, C.D. and Drazen, J.C. 2017. Spilling over deepwater boundaries: evidence of spillover from two deepwater restricted fishing areas in Hawaii. Marine Ecology Progress Series, 568, 175-190.

Sadykova, D., Scott, B.E., De Dominicis, M., Wakelin, S.L., Wolf, J. and Sadykov, A. 2020. Ecological costs of climate change on marine predator-prey population distributions by 2050. Ecology and Evolution, DOI: 10.1002/ece3.5973.

Sala-Coromina, J., Garcia, J.A., Martin, P., Fernandez-Arcaya, U. and Recasens, L. 2021. European hake (Merluccius merluccius, Linnaeus 1758) spillover analysis using VMS and landings data in a no-take zone in the northern Catalan coast (NW Mediterranean). Fisheries Research, 237, 105870.

Saraux, C., Sydeman, W., Piatt, J., Anker-Nilssen, T., Hentati-Sundberg, J., Bertrand, S., Cury, P., Furness, R.W., Mills, J.A., Österblom, H., Passuni, G., Roux, J-P., Shannon, L.J. and Crawford, R.J.M. 2020. Seabird-induced natural mortality of forage fish varies with fish abundance: evidence from five ecosystems. Fish and Fisheries doi 10.1111/faf.12517.

Sciberras, M., Hinz, H., Bennell, J.D., Jenkins, S.R., Hawkins, S.J. and Kaiser, M.J. 2013. Benthic community response to a scallop dredging closure within a dynamic seabed habitat. Marine Ecology Progress Series 480: 83-98.

Sherley, R.B., Underhill, L.G., Barham, B.J., Barham, P.J., Coetzee, J.C., Crawford, R.J.M., Dyer, B.M., Leshoro, T.M. and Upfold, L. 2013. Influence of local and regional prey availability on breeding performance of African penguins Spheniscus demersus. Marine Ecology Progress Series, 473, 291-301.

Sherley, R.B., Winker, H., Altwegg, R., van der Lingen, C.D., Votier, S.C. and Crawford, R.J.M. 2015. Bottom-up effects of a no-take zone on endangered penguin demographics. Biology Letters, 11, 20150237.

Sherley, R.B., Botha, P., Underhill, L.G., Ryan, P.G., van Zyl, D., Cockcroft, A.C., Crawford, R.J.M., Dyer, B.M. and Cook, T.R. 2017. Defining ecologically relevant scales for spatial protection with long-term data on an endangered seabird and local prey availability. Conservation Biology, 31, 1312-1321.

Sherley, R.B., Barham, B.J., Barham, P.J., Campbell, K.J., Crawford, R.J.M., Grigg, J., Horswill, C., McInnes, A., Morris, T.L., Pichegru, L., Steinfurth, A., Weller, F., Winker, H. and Votier, S.C. 2018. Bayesian inference reveals positive but subtle effects of experimental fishery closures on marine predator demographics. Proceedings of the Royal Society B Biological Sciences, 285, 20172443.

Sherley, R.B., Crawford, R.J.M., de Blocq, A.D., Dyer, B.M., Geldenhuys, D., Hagen, C., Kemper, J., Makhado, A.B., Pichegru, L., Tom, D., Upfold, L., Visagie, J., Waller, L.J. and Winker, H. 2020. The conservation status and population decline of the African penguin deconstructed in space and time. Ecology and Evolution, 10, 8506-8516.

Sherman, K., Jones, C., Sullivan, L., Smith, W., Berrien, P. and Ejsymont, L. 1981. Congruent shifts in sandeel abundance in western and eastern North Atlantic ecosystems. Nature, 291, 486–489.

Silva, T.L., Wiley, D.N., Thompson, M.A., Hong, P.T., Kaufman, L., Suca, J.A., Llopiz, J.K., Baumann, H. and Fay, G. 2020. High collocation of sand lance and protected top predators: implications for conservation and management. Conservation Science and Practice, e274, doi: 10.1111/csp2.274.

Sobel, J. and Dahlgren, C. 2004. Marine Reserves: A Guide to Science, Design, and Use. Island Press, Washington.

Sørensen, T.K., Nilsson, P. & Tullrot, A. 2009. Marine Protected Areas as a Tool for Ecosystem Conservation and Fisheries Management. https://www.ices.dk/about-ICES/projects/EU-RFP/EU%20Repository/PROTECT/FP6%20PROTECT%20Final%20Report%20Project%20Synthesis.pdf

Stanbury, A., Thomas, S., Aegerter, J., Brown, A., Bullock, D., Eaton, M., Lock, L., Luxmoore, R., Roy, S., Whitaker, S. and Oppel, S. 2017. Prioritising islands in the United Kingdom and crown dependencies for the eradication of invasive alien vertebrates and rodent biosecurity. European Journal of Wildlife Research 63: 31.

Stewart, B.D., Howarth, L.M., Wood, H., Whiteside, K., Carney, W., Crimmins, E., O’Leary, B.C., Hawkins, J.P. and Roberts, C.M. 2020. Marine conservation begins at home: how a local community and protection of a small bay sent waves of change around the UK and beyond. Frontiers in Marine Science, 7, 76.

Stobart, B., Warwick, R., Gonzalez, C., Mallol, S., Diaz, D., Renones, O. and Goni, R. 2009. Long-term and spillover effects of a marine protected area on an exploited fish community. Marine Ecology Progress Series, 384, 47-60.

Stokesbury, K.D.E. and Harris, B.P. 2006. Impact of limited short-term sea scallop fishery on epibenthic community of Georges Bank closed areas. Marine Ecology Progress Series 307: 85-100.

Studwell, A., Hines, E., Nur, N. and Jahncke, J. 2021. Using habitat risk assessment to assess disturbance from maritime activities to inform seabird conservation in a coastal marine ecosystem. Ocean & Coastal Management, 199, 105431.

Sydeman, W.J., Thompson, S.A., Anker-Nilssen, T., Arimitsu, M., Bennison, A., Bertrand, S. et al. 2017. Best practices for assessing forage fish fisheries-seabird resource competition. Fisheries Research, 194, 209-221.

Szostek, C.L., Murray, L.G., Bell, E., Rayner, G. and Kaiser, M.J. 2016. Natural vs. fishing disturbance: drivers of community composition on traditional king scallop, Pecten maximus, fishing grounds. ICES Journal of Marine Science 73: 70-83.

Thrush, S.F., Hewitt, J.E., Cummings, V.J. and Dayton, P.K. 1995. The impact of habitat disturbance by scallop dredging on marine benthic communities: What can be predicted from the results of experiments? Marine Ecology Progress Series 129: 141-150.

Tien, N.S.H., Craeymeersch, J., van Damme, C., Couperus, A.S., Adema, J. and Tulp, I. 2017. Burrow distribution of three sandeel species relates to beam trawl fishing, sediment composition and water velocity, in Dutch coastal waters. Journal of Sea Research 127: 194-202.

Vandeperre, F., Higgins, R.M., Sanchez-Meca, J., Maynou, F., Goni, R., Martin-Soza, P. et al. 2011. Effects of no-take area size and age of marine protected areas on fisheries yields: a meta-analytical approach. Fish and Fisheries, 12, 412-426.

van der Molen, J. and Pätsch, J. 2022. An overview of Atlantic forcing of the North Sea with focus on oceanography and biogeochemistry. Journal of Sea Research 189: 102281.

van Deurs, M., van Hal, R., Tomczak, M.T., Jonasdottir, S.H. and Dolmer, P. 2009. Recruitment of lesser sandeel Ammodytes marinus in relation to density dependence and zooplankton composition. Marine Ecology Progress Series 381: 249-258.

van Deurs, M., Christensen, A., Frisk, C. and Mosegaard, H. 2010. Overwintering strategy of sandeel ecotypes from an energy/predation trade-off perspective. Marine Ecology Progress Series 416: 201-215.

van Deurs, M., Christensen, A. and Rindorf, A. 2013. Patchy zooplankton grazing and high energy conversion efficiency: ecological implications of sandeel behavior and strategy. Marine Ecology Progress Series 487: 123-133.

van Deurs, M., Jorgensen, C. and Fiksen, O. 2015. Effects of copepod size on fish growth: a model based on data for North Sea sandeel. Marine Ecology Progress Series 520: 235-243.

Vilas, D., Coll, M., Corrales, X., Steenbeek, J., Piroddi, C., Calo, A., Di Franco, A., Font, T., Guidetti, P., Ligas, A., Lloret, J., Prato, G., Sahyoun, R., Sartor, P. and Claudet, J. 2020. The effects of marine protected areas on ecosystem recovery and fisheries using a comparative modelling approach. Aquatic Conservation: Marine and Freshwater Ecosystems, 30, 1885-1901.

Walton, D., 2008. Informal logic: A pragmatic approach. Cambridge University Press.

Weber, S.B., Richardson, A.J., Brown, J., Bolton, M., Godley, B.J., Leat, E., Oppel, S., Shearer, L., Soetaert, K.E.R., Weber, N. and Broderick, A.C. 2021. Direct evidence of a prey depletion “halo” surrounding a pelagic predator colony. PNAS 118: e2101325118.

Weller, F., Cecchini, L-A., Shannon, L., Sherley, R.B., Crawford, R.J.M., Altwegg, R., Scott, L., Stewart, T. and Jarre, A. 2014. A system dynamics approach to modelling multiple drivers of the African penguin population on Robben Island, South Africa. Ecological Modelling, 277, 38-56.

Wischnewski, S., Fox, D. S., McCluskie, A. & Wright, L.J. 2017. Seabird tracking at Assessing the Flamborough & Filey Coast: the impacts of offshore wind turbines. RSPB Centre for Conservation Science Report to Ørsted.

Wojczulanis-Jakubas, K., Araya-Salas, M. and Jakubas, D. 2018. Seabird parents provision their chick in a coordinated manner. PLoS ONE 13: e0189969.

Woodward, I., Thaxter, C.B., Owen, E. and Cook, A.S.C.P. 2019. Desk-based revision of seabird foraging ranges used for HRA screening. BTO Research Report No. 724.

Wright, P.J., Orpwood, J.E. and Scott, B.E. 2017. Impact of rising temperature on reproductive investment in a capital breeder: the lesser sandeel. Journal of Experimental Marine Biology and Ecology 486: 52-58.

Zupan, M., Bulleri, F., Evans, J., Fraschetti, S., Guidetti, P. et al. 2018. How good is your marine protected area at curbing threats? Biological Conservation, 221, 237-245.

 

ANNEX A. Review of Marine Protected Areas

The effectiveness of Marine Protected Areas

  1. Compensation measures may be needed for SPA seabird populations due to predicted impacts from the Proposed Development. One of the potentially beneficial measures would be to improve the demographic parameters of seabird populations predicted to be impacted by the Proposed Development through the closure or management of fisheries of seabird prey species. Additionally, the influence of prey fish abundance on seabird demographics was also reviewed.
  1. There are numerous reviews of the evidence that protected areas benefit conservation of species, communities and ecosystem services. In particular, fishery closures strongly promote the recovery of fish stock biomass following heavy exploitation (MacNeil et al. 2015, Cabral 2020). Fishery closures can take the form of technical measures (specified constraints on gear use within a fishery; McClanahan et al. 2014, Campbell et al. 2018), periodic or seasonal closures (Cohen and Alexander 2013), or rights-based controls on access into the fishery. Such constraints on fishing may be the most effective measures to achieve conservation objectives of marine protected areas (MPAs) (Campbell et al. 2018, Cabral et al. 2020, Vilas et al. 2020).
  2. From analysis of 87 MPAs worldwide, Edgar et al. (2014) defined five key factors that determine the effectiveness of an MPA; the extent to which fishing is limited, the level of enforcement of fisheries constraints, MPA age, MPA size, and presence of continuous habitat allowing spill over of fish or shellfish from the MPA into surrounding waters. Similarly, Zupan et al. (2018) found that the designation of MPAs alone may not result in the lessening of some human threats, which is highly dependent on management goals and the related specific regulations that are adopted. They showed that fully protected areas effectively eliminated extractive activities, whereas the intensity of artisanal and recreational fishing within partially protected areas they investigated, paradoxically, was higher than that found outside MPAs, questioning their ability to reach conservation targets. They concluded that understanding the intensity and occurrence of human threats operating at the local scale inside and around MPAs is important for assessing MPA effectiveness in achieving the goals they have been designed for, informing management strategies, and prioritizing specific actions.
  3. Baskett and Barnett (2015) concluded in relation to fishery no-take protected areas “Responses at each level depend on the tendency of fisheries to target larger body sizes and the tendency for greater reserve protection with less movement within and across populations. The primary population response to reserves is survival to greater ages and sizes plus increases in the population size for harvested species, with greater response to reserves that are large relative to species' movement rates. The primary community response to reserves is an increase in total biomass and diversity, with the potential for trophic cascades and altered spatial patterning of metacommunities. The primary evolutionary response to reserves is increased genetic diversity, with the theoretical potential for protection against fisheries-induced evolution and selection for reduced movement.” The potential for the combined outcome of these responses to buffer marine populations and communities against temporal environmental heterogeneity has preliminary theoretical and empirical support. However, while the benefits from many MPAs have been widely recognised, not all MPAs have successful outcomes. Giakoumi et al. (2018) reviewed 27 detailed case studies from around the world and concluded that the most important factor determining the success or failure of a MPA was the level of stakeholder engagement. This conclusion was also reached in a comparison between two MPAs for coral reef fish in the Philippines, one successful and one unsuccessful, because constraints on fishing failed at one site due to a lack of community support (Russ and Alcala 1999).
  4. As one recent example in the context of fishery impacts, Fernandez-Chacon et al. (2020) studied MPA effects on lobsters Homarus gammarus collected at three pairs of MPA and control areas in Norway and reported that “annual mean survival was higher inside MPAs (0.592) vs. control areas (0.298), that significant negative relationships between survival and body size occurred at the control areas but not in the MPAs, where the effect of body size was predominantly positive. Additionally, we found that mean and maximum body size increased over time inside MPAs but not in control areas. Overall, our results suggest that MPAs can rebuild phenotypic complexity (i.e. size structure) and provide protection from harvest selection”.
  5. Jaco and Steele (2019) showed that MPA effects on fish size and survival were greater where prior fishing pressure had been higher, a conclusion also reached by Buxton et al. (2014). This does make the point that selecting areas for protection will have the greatest benefit where the impact of fishing mortality can be reduced most.
  6. Ballantyne (2014) reviewed the results from establishment of marine protected areas in New Zealand waters since the first was designated in 1977. He concluded, “When marine reserves were established, their ecology began to change, due to the cessation of fishing and other previous manipulations. These changes were complex, often large and continued to develop for decades. The study of these changes, and a continuing comparison to fished areas provided a great deal of new scientific data showing how fishing directly and indirectly alters ecosystems. The scientific benefits of marine reserves proved so numerous that it became clear that marine reserves are as important to science - they are the controls for the uncontrolled experiment that is happening due to fishing and other human activities. The general benefits of marine reserves to society as a whole; directly to conservation, education, recreation and management, and indirectly to fisheries, tourism and coastal planning; are so important that a systematic approach to their creation is in the public interest”.
  7. Parsons et al. (2004) reported long-term effects of protection within the Leigh marine reserve, New Zealand, including a trophic cascade related to predator activity with recovery of kelp forest in waters <8 m deep, and increase in turfing algal habitat. Snappers Pagrus auratus have been actively fished for more than 100 years in New Zealand and studied by fisheries scientists for more than 50 years. However, when studied in the marine reserve at Leigh (where it had become sixteen times more abundant than in fished areas outside the reserve, suggesting a change in ranging behaviour in response to the lack of fishing) it was discovered that, within the reserve, most individuals had small home-ranges in which they stayed for months at a time (Parsons et al. 2003).
  8. The Tsitsikamma National Park Marine Protected Area (Tsitsikamma MPA), a 60 km stretch of exposed rocky southern coast of South Africa, was proclaimed in 1964, making it Africa’s oldest MPA. This site was established as a zone with fishing strictly limited by permit, to try to recover over-exploited stocks of reef fish, many of the species present being endemic to South Africa. Many of these fish species have maximum ages over 20 years and are highly resident, so appear suited to protected area conservation. Tsitsikamma MPA has been a focus of research testing the hypothesis that MPAs allow recovery of depleted stocks of reef fish and the maintenance of critical spawner biomass. Despite extensive illegal poaching of fish from within this MPA, and several changes over the decades in the severity of constraint on fishing (Lombard et al. 2020), Buxton and Smale (1989) showed that roman Chrysoblephus laticeps, dageraad Chrysoblephus cristiceps and red steenbras Petrus rupestris achieved greater abundance and sizes inside the MPA than outside. Cowley et al. (2002) recorded that blacktail Diplodus capensis, zebra D. hottentotus, bronze bream Pachymetopon grande and galjoen Dichistius capensis achieved abundances of 5 to 21 times more inside the MPA than outside, and that these fish were on average 40% larger in the MPA than outside.
  9. Malcolm et al. (2018) used stereo baited remote underwater videos eight, nine, thirteen and fourteen years after ‘no take’ marine protected areas were established at the Solitary Islands Marine Park, Australia. Four species targeted by fishers: snapper Chrysophrys auratus, grey morwong Nemadactylus douglasi, pearl perch Glaucosoma scapulare, and venus-tuskfish Choerodon venustus, were more abundant and larger in ‘no take’ zones and showed an increase through time in ‘no take’ relative to fished areas. In contrast, there was no distinct pattern of four bycatch species increasing in abundance in ‘no-take’ areas.
  10. Boulcott et al. (2018) reported on the abundances of scallops in a small, protected area in Lamlash Bay, Arran. A no-take zone (NTZ) was established in 2008 in a small area (about 2.7 km2) of Lamlash Bay, excluding scallop dredging and bottom-trawling from the area. Five years after the closure, there was neither a significant increase in adult scallop abundance within the NTZ nor evidence of the dispersal of adults into surrounding areas. That finding contradicts an earlier claim that this NTZ had resulted in higher recruitment of scallop larvae into the NTZ compared to densities found outside the NTZ (Howarth et al. 2011). Boulcott et al. (2018) concluded that the small size of the NTZ may have played a role in the lack of demonstrable scallop recovery, that the lack of an effect may also be due to relatively low fishing pressure before the no-take zone was established, and that possibly responses may take more than five years in species where high recruitment is infrequent, as is the case in scallops. However, by 2019 the density of king scallops in the NTZ had increased substantially, to more than 3.7 times the level in 2013, and to a significantly higher abundance than in areas outside the NTZ (Stewart et al. 2020).
  11. Abundances of the European lobster Homarus gammarus in Lamlash Bay NTZ (Howarth et al. 2016) and in a similar‐sized NTZ in Lundy, UK (Hoskin et al. 2011), were found to increase demonstrably within 2–3 years of the closure of fishing within the NTZ. However, Howarth et al. (2016) concluded that high fishing effort outside the reserve may have reduced lobster abundance towards the end of their study, further supporting the concern about the effectiveness of a NTZ that is small in relation to the dispersal movements of the animals. Lobster Catch Per Unit Effort (CPUE) declined with increasing distance from the NTZ boundaries up to 20 km away (Howarth et al. 2016). Tagging and recapturing of the lobsters indicated this was likely due to “spillover”, with individuals from within the NTZ moving outside (Howarth et al. 2016, Stewart et al. 2020). The body size of lobsters was also consistently greater within the NTZ across all years, and because egg production increases with body size, and mature lobsters were so much more abundant in the NTZ, this difference translated to over 5.7 times more eggs within the NTZ in 2018, than in an unprotected area of equal size (Stewart et al. 2020). Stewart et al. (2020) concluded that “Our results demonstrate that recovery of biological communities inside protected areas is not monotonic; instead, what we are seeing is complex, ecological processes unfolding in a dynamic environment. This should not be seen as problematic; the complexity should be embraced; it is a more accurate reflection of how ecosystems naturally function. This emerging understanding is crucial for both setting realistic management objectives for other MPAs in the region, and for managing the expectations of conservationists and managers in the future”.
  12. Kough et al. (2019) showed that Exuma Cays MPAs held higher densities of queen conch Lobatus gigas than found in fished areas and showed that there are positive associations between enforcement and conch size and age. They concluded that the MPA is currently sustaining the nearby populations exposed to fishing, as a result of spillover of larvae from the MPA.
  13. One of the key objectives of MPAs is to create “spillover” with fish or crustaceans that increase in density in the MPA dispersing into adjacent areas. Many studies present evidence that spillover occurs from MPAs and so supports fisheries in the region (e.g. McClanahan and Mangi 2000, Gell and Roberts 2003, Abesamis and Russ 2005, Goni et al. 2008, Harmelin-Vivien et al. 2008, Stobart et al. 2009, Goni et al. 2010, Vandeperre et al. 2011, Florin et al. 2013, Huserbråten et al. 2013, Kerwath et al. 2013, Rossiter and Levine 2014, Alos et al. 2015, Di Lorenzo et al. 2016, Sackett et al. 2017, Kleiven et al. 2019, Kough et al. 2019, Marshall et al. 2019, Cabral et al. 2020, Di Lorenzo et al. 2020, Vilas et al. 2020, Sala-Coromina et al. 2021). For example, Huserbråten et al. (2013) showed that European lobster Homarus gammarus survival and abundance and size increased in MPAs where fishing for lobsters was prohibited. They also showed that there was some spillover of adult lobsters, but that this was very limited due to high levels of residency of these animals. However, larval export from the MPAs was assessed as being very high, and therefore affecting large areas outside the small MPAs due to the pelagic larval stage. Spillover of larvae can be especially important from MPAs because the mean size of fish or crustacea tends to increase within MPAs, and larger animals produce disproportionally greater numbers of larvae (Marshall et al. 2019).
  14. Kleiven et al. (2019) presented results from a fine-scale spatial gradient study conducted before and after the implementation of a five km2 lobster MPA in southern Norway. A significant nonlinear response in lobster abundance, estimated as CPUE from experimental fishing, was detected within two years of protection. After four years, CPUE values inside the MPA had increased by a magnitude of 2.6 compared to before-protection values. CPUE showed a significant nonlinear decline from the centre of the MPA, with a depression immediately outside the border and a plateau in fished areas. Overall fishing pressure almost doubled over the course of the study. The highest increase in fishing pressure (by a magnitude of 3) was recorded within one km of the MPA border, providing a plausible cause for the depression in CPUE. The authors conclude that, taken together, these results demonstrate the need to regulate fishing pressure in surrounding areas when MPAs are implemented as fishery management tools.
  15. Stobart et al. (2009) reported that at the Columbretes Islands Marine Reserve, Spain, relative to nearby fished areas the reserve fish community had higher abundance and biomass, and larger relative body size. They found clear evidence of spillover of fish from the reserve to the adjacent fishery as commercial fish yields at the reserve border increased continuously during the study period, despite being locally depleted due to fishing effort concentration at the edge of the reserve (“fishing the line”). Harmelin-Vivien et al. (2008) assessed the presence of gradients of fish abundance and biomass across marine reserve boundaries in six Mediterranean MPAs. A reserve effect was detected, with higher values of fish species richness (x1.1), abundance (x1.3), and biomass (x4.7) recorded inside MPAs compared to adjacent fished areas. Linear correlations revealed significant negative gradients in mean fish biomass in all the reserves studied. They concluded that the existence of regular patterns of negative fish biomass gradients from within MPAs to fished areas was consistent with the hypothesis of adult fish biomass spillover processes from marine reserves, and that it could be considered as a general pattern in the Mediterranean region. Vandeperre et al. (2011) used 28 data sets from seven MPAs in southern Europe to show that CPUE of fisheries outside the MPAs increased as a result of spillover of fish from the MPA. Furthermore, the boost to the marketable catch from spillover increased by an average of 3% per year for at least 30 years after designation of the MPAs.
  16. Using a 15-year time series of nationwide, spatially referenced catch and effort data, Kerwath et al. (2013) found that the establishment of the Goukamma MPA benefited the adjacent fishery for roman Chrysoblephus laticeps, a South African endemic seabream. Roman-directed CPUE in the vicinity of the new MPA immediately increased, contradicting trends across this species’ distribution. The increase continued after 5 years, the time lag expected for larval export, effectively doubling the pre-MPA CPUE after 10 years. Garcia-Rubies et al. (2013) point out that spillover may not occur in the initial stages of some MPAs, especially where fish are slow-growing and long-lived so may take many years to reach carrying capacity within the MPA, and significant spillover of adult or maturing fish is only likely after that has occurred.
  17. Di Lorenzo et al. (2020) developed a meta-analysis of a global database covering 23 MPAs where fishing is prohibited or strictly limited, in twelve different countries, to assess the capacity of MPAs to export fish biomass and to assess whether this response was mediated by particular MPA features (e.g. size, age) or fish species characteristics (e.g. mobility, economic value). Results, on average, showed that fish biomass and abundance were highest inside the MPA, but outside the MPAs were higher in locations close to MPA borders, were particularly higher close to the MPA for species with a high commercial value, and were higher in the presence of a partially protected area (PPA) surrounding the MPA. Spillover slightly increased as MPAs were larger and older and for species that were more mobile. The authors concluded that spillover is a regular feature of MPAs where fishing is prohibited or limited, and that this could enhance local fishery management.
  18. While there is much empirical evidence of increases in sizes and numbers of animals within MPAs compared with control areas outside the MPA, another approach to assessing the benefits of MPAs is to use scenario modelling. Dahood et al. (2020) used a dynamic food web model to evaluate a range of different scenarios for MPAs in the Southern Ocean. Halouani et al. (2020) used a modelling approach to assess the extent to which the ‘no-take zone’ created by an offshore wind farm may benefit conservation of fish stocks. Vilas et al. (2020) used a comparative food-web modelling approach to demonstrate that fully protected MPAs perform better than partially protected MPAs and, even when small, can yield local positive impacts on the structure and functioning of marine ecosystems that contribute to support local fisheries.
  19. The success of very many MPAs and NTZs around the world has led to a more strategic approach to marine conservation designations in some countries. In 2002, after more than a decade of consultation, the State of Victoria, Australia, established 24 no-take areas (including 10 Marine National Parks) totalling 540 km2 and more than 5% of State waters (Sobel and Dahlgren 2004). This was the world’s first representative system of marine reserves. In 2003, the California Fish and Game Commission approved ten ‘no-take’ marine reserves in the northern Channel Islands, California. The initial zones covered state waters (out to three nautical miles), but later the federal authorities extended these to six nautical miles. The reserves comprised 25% of waters around the islands and formed the first replicated and representative marine reserve system. In 2004, the Great Barrier Reef Marine Park Authority’s new zoning plan was approved by the Australian Federal Government (Sobel and Dahlgren 2004). The plan required a minimum of 25% by area of all 73 bioregions in the Great Barrier Reef Marine Park to be completely ‘no-take’.
  20. On the high seas, 286,200 km2 of the North-East Atlantic was designated as six MPAs in international waters under the Convention for the Protection of the Marine Environment of the North-East Atlantic (the OSPAR Convention) in 2010, which is considered to be the start of a process of developing an ecologically coherent and representative MPA network in that ocean (O’Leary et al. 2012).
  21. In England, in addition to existing and new SPAs and SACs, 91 Marine Conservation Zones (MCZs) have been designated between November 2013 and May 2019 as an ecologically coherent network in terms of representation of species and habitats. In Scotland, a combination of marine extensions to Special Protection Areas (SPAs) originally designated for breeding seabirds, designation of marine areas as SPAs for nonbreeding seabirds, designation of SACs for marine mammals, MPAs for marine mammals, fish and marine invertebrates, comprise 225 sites providing protection over more than 37% of Scotland’s marine waters. Many of these sites have been designated within the last few years, so too recently for any assessment of changes that may follow as a consequence of management. Not all of these MPAs involve establishment of fisheries restrictions, depending on the objectives for individual sites. In addition to SPAs, SACs and MPAs, five other area-based measures include a temporary no-take zone for sandeel fishing off east Scotland, which has remained in force without any suggestion that this will be revoked.
  22. The efficacy of MPAs might be compromised by climate change if climate change results in the poleward shift of species’ distributions so could move species out of MPAs. While modelling of species’ distributions suggests such poleward shifts will occur (Sadykova et al. 2020, Clairbaux et al. 2021), the key feature of MPAs is the reduction in fishing pressure on stocks. There will be few cases where MPAs are situated at the equatorial edge of fish distributions, so climate change is unlikely to negate the benefits of MPAs except in a very few exceptional such cases (Clairbaux et al. 2021).

Case studies of NTZs that influence seabird demography

  1. Very few MPAs/NTZs have been designated with the objective to enhance conservation of seabird populations (Ronconi et al. 2012, Hentati-Sundberg et al. 2020). However, that outcome could arise if MPA/NTZ designation resulted in a reduction of seabird bycatch in fisheries, or if the MPA/NTZ resulted in a bottom-up increase in energy flow through the food web up to seabirds (i.e. increased the abundance or quality of their preferred foods; Hentati-Sundberg et al. 2020), or if MPA/NTZ designation improved the quality of breeding habitat for seabirds (for example by reducing human disturbance, removing threats from alien invasive mammal predators, or improving nest site quality).
  2. Several studies have focused on the potential of designating or managing marine protected areas for seabird conservation (Lascelles et al. 2012, Ronconi et al. 2012, Sherley et al. 2017). Studwell et al. (2021) presented a habitat prioritization approach for identifying critical areas for wildlife conservation action, including seabirds. They demonstrated the value of that approach by applying it to the wildlife in the offshore waters of Greater Farallones National Marine Sanctuary and Cordell Bank National Marine Sanctuary, California. They identified areas where seabirds would benefit from a combination of adding protections to some areas and enhancing management of the primary disturbance resulting from higher risk activities, which in their case study included benthic fishing with mobile or fixed gear. Silva et al. (2020) investigated spatial overlap between a key forage fish species (sandeel) and two protected predators, humpback whale and great shearwater in the Gulf of Maine, USA. Both the cetacean and the seabird showed very strong and consistent match in spatial distribution with that of sandeel. They proposed managing protected areas for these top predators on the basis of the key role of sandeel habitat in determining predator distributions in that system.
  3. In a review of the pressures and threats to global populations of penguins, Boersma et al. (2020) identified marine spatial planning as the highest ranked conservation need to conserve endangered penguin populations, for which they particularly emphasize the need for MPAs to manage fisheries to ensure that adequate prey resources for penguins remain in areas critical to their breeding success (i.e. close to colonies) and survival (i.e. over larger spatial scales when penguins are dispersed from the colony sites).
  4. Requena et al. (2020) used tracking data from nine seabird species and one marine mammal to identify marine hotspots around Tristan da Cunha, South Atlantic Ocean. These included offshore sea mounts as well as areas in the vicinity of breeding sites on the islands and were consistent across years. They concluded that tracking data provide reliable information that could be used to define MPAs for these top predator populations, which include several endemic and globally threatened species. Analyses of seabird tracking data in UK waters was considered to provide effective identification of seabird hotspots that could be designated as MPAs (Cleasby et al. 2020). Using maximum curvature methods (as developed for seabird hotspot identification by O’Brien et al. 2012) allowed clear definition of seabird hotspots and this and other analytical methods consistently identified several high-density areas that Kober et al. (2010) and Cleasby et al. (2020) considered should be prioritised for seabird conservation. Critchley et al. (2019) used seabird tracking data to test whether simple foraging radius models from colonies provide a cost-effective alternative to large-scale surveys or tracking studies. They showed that for a range of seabirds of differing ecology (razorbill, puffin, Manx shearwater and European storm-petrel) foraging radius distribution broadly matched foraging areas identified from tracking breeding adults from colonies or from aerial surveys. The foraging radius method fitted better to tracking data than to aerial survey data, which could indicate that nonbreeding birds that will be seen in aerial survey data but not in tracking data and which represent a significant component of the total population but may avoid areas with dense aggregations of more experienced breeding adults, may confuse efforts to identify key foraging areas used by breeding birds. Perrow et al. (2015) also used a combination of tracking of breeding adults, a boat-based survey, and a foraging radius approach to define the at-sea MPA (in this case a SPA marine extension) for breeding little terns. They also found that these different approaches defined areas that were broadly similar, giving confidence in the use of each and suggesting that an integrated approach would be most suitable. Similarly, tracking data from marine mammals have been used to justify decisions on boundaries of MPAs, in some cases providing retrospective justification (e.g. Kirkman et al. 2016). Arias-Del-Razo et al. (2019) showed that MPAs with large populations of marine mammals still provided large gains in fish biomass (which increased with the age of the MPA), despite the presence of marine mammals that could be a major predator on those fish. However, Kelaher et al. (2015) concluded that reef fish increased less in MPAs with large seal populations than in MPAs without large numbers of seals and suggested that if the aim is to recover reef fish populations, designating MPA sites away from seal colonies may be preferable. An implication of this, of course, is that if the aim is to improve conditions for top predators, then marine habitat management that enhances populations of fish on which the predators can feed will be an effective conservation measure.
  5. Bertrand et al. (2012) showed that the foraging efficiency of breeding seabirds in Peru may be significantly affected by not only the global quantity, but also the temporal and spatial patterns of fishery removals of forage fish (in this case, anchoveta). They concluded that, together with an ecosystem-based definition of the fishery quota, an ecosystem approach to fisheries management should limit the risk of local depletion around breeding colonies using, for instance, adaptive marine protected areas around colonies of forage-fish dependent seabirds.
  6. Hentati-Sundberg et al. (2020) developed a bioenergetics model linking top predator (such as seabirds) breeding biology and foraging ecology with forage fish ecology and fisheries management. They applied their framework to the case study example of common guillemots and razorbills at a Baltic Sea colony where they depend on sprat and juvenile herring as key prey species. They showed that a fishery management target of ‘one-third-for-the-birds’ (Cury et al. 2011) is sufficient to sustain successful breeding by the seabirds. However, the results also highlight the importance of maintaining sufficient prey densities in the vicinity of the colony, suggesting that fine-scale spatial fisheries management is necessary to maintain high seabird breeding success, and therefore indicating the value of a MPA that limits forage-fish fishery harvests in areas close to the seabird colony.