Studies of no-take marine reserves around the world have suggested that, on average, total biological diversity inside reserves is higher than outside. That said, within a designated marine reserve over time, each species or group of species can respond by increasing in population, decreasing in population, or having no response at all. The response depends on a range of factors, including predator-prey relationships. In cases where a reserve protects a predator species, an increase in predator abundance can in turn decrease the numbers of prey in the reserve – either through direct predation or predator-avoidance behavior by the prey. These shifts can have ecosystem-wide effects, with indirect impacts on biodiversity within reserves or, in theory, on fish stocks outside.

The complex linkages in ecological communities, particularly predator-prey relationships, make it challenging to predict the indirect outcomes of reserve creation. However, planners can gain an appreciation for potential effects by learning from what has occurred in reserves elsewhere. This month, MPA News examines how increases in predator populations can affect the goals of marine reserves, and how planners can prepare for these effects.

Impacts of predators on biodiversity reserves

A frequent goal of marine reserves is to increase biodiversity by removing exploitation pressure. Expecting increases in all species following reserve designation is unrealistic, owing to the various factors contributing to each species’ response: the level of exploitation, life-history characteristics, potential for replenishment from surrounding areas, and abundance of predators and prey. The ecological interactions that play out in a reserve can yield unexpected results.

“It is certainly true that it can be difficult to predict the impact of protecting one group of animals on others elsewhere in the system,” says John Pinnegar, a biologist at the UK-based Centre for Environment, Fisheries & Aquaculture Science (CEFAS) who has studied predatory interactions in MPAs and non-protected areas worldwide. In a review of research at 21 sites, he documented 39 cases of what he called “trophic cascades”, in which the presence of primary carnivores had suppressed herbivores, thereby increasing plant abundance. (Trophic cascades can occur in reverse in cases of overfishing: primary carnivores are removed, thus increasing herbivores and suppressing plant growth. They can also occur among levels of carnivores with little or no effect on plants.)

Pinnegar’s study, which he conducted with a team of researchers from Mediterranean countries and published in Environmental Conservation (27:2 [179-200]), pointed out that large predatory species are often the most susceptible to fishing. Therefore their recovery in reserves would be expected to have top-down effects on other species.

Examples of trophic cascades in reserves from around the world, cited in Pinnegar’s study and elsewhere, include:

Malindi, Kisite, and Watamu Marine National Parks, Kenya: Triggerfish, considered the most important predator of sea urchins in Kenya, are protected in these national parks but depleted in adjacent fished areas. In the depleted areas, urchins have tended to become the dominant grazer. This has led to increases in urchin-resistant turf algae and decreases in hard coral cover, with the latter due in part to urchin grazing (coral damage from fishing gear is also a factor). The implication is that where Kenyan reefs are protected from fishing, triggerfish abundance will increase, sea urchin and turf-algal abundance on reef flats will decline, and coral cover will correspondingly increase.

Leigh Marine Reserve, New Zealand: Abundance of predatory fish and spiny lobsters is significantly higher inside this temperate reserve than in adjacent fished areas. Densities of sea urchins, a component in the diet of the fish and lobsters, have declined since the reserve’s designation in the 1970s. As a result, kelp – which the urchins normally graze – has increased in cover.

Brackett’s Landing Conservation Area, US: Over a seven-year time span, densities of predatory copper rockfish declined substantially in this reserve in Washington State, while densities of lingcod – a larger predator – increased. Each species is targeted by fishermen outside the reserve. Researchers suggest these patterns may have occurred due to direct predation by lingcod on rockfish (a known behavior) or lingcod outcompeting rockfish for prey items. (This cascade has had no significant effect on primary production.)

The simplicity of these examples may be deceptive. Rarely are trophic cascades the only factor dictating ecosystem effects. In the case of Brackett’s Landing, evidence of the decline in rockfish became apparent in the late 1990s, a quarter-century after the reserve was designated. Until then, rockfish and lingcod had both been relatively abundant in the reserve. Why would this balance between lingcod and rockfish suddenly shift? Regional fisheries management may have played a role: fishing limits instituted for lingcod in the 1980s and ’90s, along with improved recruitment, have helped its populations to increase region-wide. In the reserve, perhaps the growing lingcod population reached a tipping point past which rockfish could no longer co-exist as effectively. Researchers are unsure.

“Nature is complicated, and we should not expect to predict the response to reserves in all situations,” says Tim McClanahan, a biologist with the US-based Wildlife Conservation Society who conducted the Kenyan research on coral, urchins, and triggerfish. Nonetheless, he adds, it is possible to draw some generalizations about recovery. “Reserves will often produce fairly fast recovery for some of the key target fisheries species, so it should not be hard to see early recoveries for these species,” he says as an example. “There are, however, a number of species and groups that are slow to recover and may take more than 10 years to reach their undisturbed levels.”

McClanahan suggests that it is nature’s complexity itself that necessitates the designation of no-take reserves. “Reserves provide the pieces for nature’s self-organization,” he says. Without unfished areas – which theoretically allow an ecosystem to re-approach its original, “natural” state over time – there would be little way for researchers to avoid the sliding baseline phenomenon, in which expectations of what is natural are skewed because many of the original components of the system are reduced or absent. Marine reserves – including the unforeseen effects they can exhibit – change the benchmarks for environmental and fisheries management, reflecting a natural state that managers and researchers may not have observed in their lifetimes.

The naturalness of reserves was part of the rationale behind plans to re-zone the Great Barrier Reef Marine Park, says Leanne Fernandes, manager of the park’s Representative Areas Program (RAP). RAP resulted in greatly expanded no-take areas for the park, effective 1 July (MPA News 5:10). “One of the reasons for the increased level of protection was to move the system as a whole – especially within the no-take areas – toward a higher level of natural integrity,” she says. “Preventing the take of target species, and of bycatch, has the flow-on effect of helping to restore the natural integrity of the local food webs.” That integrity, she says, will hopefully provide resilience to other pressures on the system, such as climate change. Monitoring the effects of the new reserves will require study of target and non-target species and habitat changes over time.

Fernandes acknowledges that trophic cascade effects are significant but poorly understood, and that implementing the new network of no-take areas on the Great Barrier Reef may have unforeseen impacts on the system as a whole. But that is part of returning the system to a more natural state. “In this way, trophic cascade effects were an integral part of considerations in the planning process, but it didn’t mean that the design was specifically altered in some way to accommodate the concept,” she says. “It was inherent.”

Impacts of predators on fishery reserves

Where a reserve is designed to support fisheries through sustained spillover of adults into fished areas, increased abundance of predators within the reserve can limit the site’s effectiveness. If predators are consuming the same target species the fishermen are harvesting, they essentially become competitors for that prey source. Spillover of the target species decreases, and the fishermen may suffer reduced catches.

Marine mammals provide some of the best examples of this kind of predator impact. Their impact is increased where the marine mammals themselves are off-limits to hunting: in these cases, their populations are largely limited by the food resource. Around the world, it is not unusual for fishermen to complain that seals, sea lions, whales, and other marine mammals are taking their fish. In Atlantic Canada, the Canadian government expanded its harp seal hunt this year to its highest take in nearly 50 years, in part to try to limit the impact the seals are having on Atlantic cod. The Canadian cod fishery has been drastically reduced in the past decade due to overfishing, and the increased seal populations have been accused of hindering the fishery’s recovery.

Scientific understanding of competition between predators and fishermen is murky. John Pinnegar, the researcher who reviewed trophic cascades in reserves worldwide, is now studying predator-prey interactions in the North Sea and cites several studies in which changes in model configuration provided different conclusions on the utility of seal hunts for protecting fisheries. In one study, when two prey species were aggregated in the model, a seal hunt was recommended; then, when the prey species were considered separately, complete protection of seal stocks was recommended. “This was because of indirect predator-prey and competition effects,” he says. “You have to be very careful about the assumptions of your models.” In his current research, Pinnegar is studying whale-fishery interactions and the problems encountered with different model formulations.

Inspired by a proposed marine national park off the coast of Brittany in France, Jean Boncoeur, an economist at the Universite de Bretagne Occidentale, modeled potential interactions not only among fish, seals, and fishermen in the area, but also their interaction with tourists. He wanted to determine the economic consequences of creating a marine reserve in which fishing adjacent to the reserve and ecotourism (seal watching) were both considered, and how these consequences could inform the size of the reserve.

His findings: the optimal reserve size, according to a global cost-benefit analysis, was larger than the one that would be optimal if fisheries management were the only objective. This was because the growth in the seal stock generated by a larger reserve increased the opportunity to make money through ecotourism (the number of tourist visits was assumed to be an increasing function of the seal stock). In fact, because the model also assumed tourism to generate more net regional income than fishing, any and all increases in reserve size and seal stocks resulted in improved overall efficiency of the reserve, although much of the improvement was realized to the detriment of the fishing industry (from decreased fishing area and increased competition with seals). Boncoeur submitted the research results to planners of the Iroise Sea National Park in 2000. The park is still under development.

In research published in Conservation Biology in 2003 (17:1[273-283]), a US research team studied several MPAs along the California coast to compare the effects of a top predator – sea otters – with the effects of human recreational harvest on red abalone, a commercially valuable mollusk eaten by otters. What they sought was insight on whether MPAs intended to conserve ecosystems, including sea otters, were compatible with the use of MPAs for abalone fishery sustainability. (Abalones have been prone to boom and bust fisheries, while otters are recovering from severe hunting pressure in the 18th and 19th centuries. The geographic range of red abalone is wholly within the historic range of sea otters, although otters have not yet returned to their entire range in the state.)

The research team found that where sea otters were present, abalones were constrained to densities and sizes that were most likely inadequate for regional fishery sustainability. The conclusion was that MPAs off California could not enhance abalone fisheries if, in the interest of ecosystem integrity, they also contained sea otters. Thus, the researchers recommended the designation of two categories of spatially segregated, single-use MPAs: one focusing on ecosystem restoration and one on fishery development. “Species recoveries may be pleasing to ecologists and environmental advocates who yearn for the biological integrity of ecosystems but may be costly to human communities and economies,” wrote the researchers. (A change in the relative economic value of sea otters versus abalone fisheries – such as from establishment of otter-based ecotourism – could affect management decisions, akin to Boncoeur’s above-mentioned model.)

The concept of otter-free reserves for abalones begs the question of what would be done should otters find their way into these sites – as they most likely would over time. Managers would need to physically remove them, such as with culls, relocation, otter-scaring devices, or other methods. The researchers admit this would not be easy. “Such methods are either politically controversial or are of questionable effectiveness,” says Glenn VanBlaricom, a study co-author and biologist with the US Geological Survey.

Samantha Fanshawe, who collected the abalone data for the study and is now director of conservation for the UK-based Marine Conservation Society, says zoning the California coastline according to spatially explicit uses – ecosystem restoration, fishing, and other activities – would involve identifying which areas had the highest natural value, which ones had the highest fisheries value, and so on. This could have benefits beyond just otters and abalones, she says. “Identifying and mapping the distribution of these areas and where they overlap – and agreeing on where activities would be allowed or where nature takes precedence – would benefit industry as well as conservationists,” she says. “Everyone could plan their developments on a more strategic and long-term basis.”

For more information:

John Pinnegar, Centre for Environment, Fisheries & Aquaculture Science (CEFAS), Lowestoft Laboratory, Pakefield Road, Lowestoft, Suffolk, NR33 0HT, United Kingdom. Tel. +44 (0) 1502 52 4229; E-mail: j.k.pinnegar@cefas.co.uk

Tim McClanahan, Wildlife Conservation Society, Coral Reef Conservation, Kibaki Flats no.12, Bamburi, Kenyatta Beach, P.O. Box 99470, Mombasa, Kenya. Postal Code: 80107. Tel: +254 41 548 6549; E-mail: tmcclanahan@wcs.org

Leanne Fernandes, GBRMPA, PO Box 1379 Townsville, Queensland 4810, Australia. Tel: +61 7 4750 0779; E-mail: leannef@gbrmpa.gov.au

Jean Boncoeur, CEDEM/UBO, 12, rue de Kergoat – BP 816, 29285 Brest Cedex, France. Tel +33 (0)2 98 01 60 40; E-mail: Jean.Boncoeur@univ-brest.fr

Sam Fanshawe, Marine Conservation Society, Unit 3, Wolf Business Park, Alton Road, Ross-on-Wye, HR9 5NB, UK. Tel: +44 (0)1989 566017; E-mail: sam@mcsuk.org