Animal behaviour

Older but less wise

Most fish living in marine reserves are older, bigger and more fecund than those outside their borders, but they are also slower to flee a threat. The potential for 'spillover' of such fish into fisheries may boost support for reserves.

Marine reserves are designed to protect the aquatic life within their margins. It seems probable that, by providing a place for fish to grow and reproduce, they will also benefit adjacent fisheries. Writing in Ecology Letters, Januchowski-Hartley et al.1 add a new twist to this concept, by demonstrating that fish that wander over a reserve boundary into waters in which fishing occurs are more easily caught than those that have lived continuously with the threat of fishing.

Fish living in a reserve in which fishing is prohibited are expected to live longer, grow larger and have more offspring than those not so protected2. Some of these offspring will disperse naturally beyond the boundaries as eggs or larvae, in a process called recruitment subsidy; the remaining offspring generate greater fish numbers and biomass inside the reserve. This should, in turn, lead to 'spillover' — the continuous net movement of juvenile and adult individuals beyond reserve boundaries. The effects of recruitment subsidy are thought to be large and widespread because the larvae of most fish species are pelagic (they live within the water column, rather than near the bottom) and are therefore readily dispersed. By contrast, the spillover effect is expected to be restricted to sites close to the reserve boundary.

However, this eminently logical theory depends on assumptions that are seldom stated explicitly2. For this model to hold, the reserve must be large enough (or the fish sedentary enough) for individuals to experience reduced fishing pressure — a fish that wanders widely, swimming in and out of a reserve, will get little benefit. The reserve must also be well managed, so that fishing pressure within its boundaries really is lower than that outside. And the fish must produce offspring that are dispersive early in life. If these requirements are met, marine reserves should enhance fishery yields through both recruitment subsidy and spillover, and this expectation has become a commonly used argument in attempts to convince fishing communities to give up part of their fishing area for the establishment of a marine reserve.

The enthusiasm for marine reserves in the conservation community has led to strong advocacy for their use as a fishery-management tool — an advocacy effort that has jumped well ahead of the evidence that real augmentation of fishing actually results. Although the extent of this overreach has been noted several times2,3, data showing that some reserves seem not to enhance fisheries4 have been glossed over, and less-positive reports, such as one showing that the increase in marine protected areas worldwide is having no effect on the global loss of biodiversity5, can have somewhat difficult paths to publication. Nevertheless, despite the hype, there is now abundant evidence that, for reasonably sedentary species in many environments, marine reserves will contain the more abundant and older fish expected by theory2,4. Concurrently, there is growing evidence of spillover, particularly in coral-reef systems4,6, and some evidence for recruitment subsidy, in particular from a recent study of larval dispersal from marine reserves within the Great Barrier Reef Marine Park in Australia7. This study found that 55% (for stripey snapper; Lutjanus carponotatus) and 83% (for coral trout; Plectropomus maculatus) of all juveniles produced in reserves dispersed to subsidize recruitment to surrounding fishing grounds.

Now, Januchowski-Hartley and colleagues take the evidence for spillover a step further. They report that, in three Philippine locations, fish that live in the safety of a reserve are less vigilant than fish living outside the protected area, and that they bring their less-vigilant behaviour with them when they wander across a reserve boundary.

The researchers looked at the behaviour of three families of reef fish: butterflyfish (Chaetodontidae), which are not a target for fishing, and surgeonfish (Acanthuridae) and parrotfish (Scaridae), which are fishery targets (Fig. 1). The study design involved spotting individual fish engaged in feeding or swimming behaviour (not in social activities). A snorkeller (Januchowski-Hartley) would then descend to about 8–10 metres away from the fish, and swim towards it at constant slow speed. When the fish fled or sought shelter among the coral, the snorkeller recorded the linear distance between himself and the fish just before it fled — the flight initiation distance (FID). The authors also recorded the estimated total length of the fish. They classified each encounter as within one of eight 50-metre-wide zones that spanned from 200 m inside to 200 m outside the reserve boundary. Finally, they repeated the same procedure around control 'boundaries' within the fishing zone and away from marine reserves.

Figure 1: Beyond the boundaries.
figure1

REINHARD DIRSCHERL/FLPA

Januchowski-Hartley et al.1 compared the behaviour of fish species that are targets for fishing, including surgeonfish (such as Naso vlamingii, shown) and parrotfish, with non-targeted butterflyfish. They show that the flight initiation distance — the distance between a fish and an approaching snorkeller at which the fish flees — is smaller for targeted species in marine reserves than for those in fisheries. Moreover, this distance increases with increasing distance from the reserve boundary. No difference in flight behaviour was observed in the non-targeted species.

The main results are straightforward: the FID increased for each of the two fished families in all three reserves as the location of the encounters moved from inside to outside the boundary. No such trend was seen across control boundaries or for the non-fished butterflyfish. Because fish are easier to spear if they have a shorter FID, these results mean that fish just outside the boundary of a marine reserve will be easier to catch (at least by spearfishing) than those farther from the boundary.

The obvious explanation is that fish learn to adjust their FID according to the level of risk, that FIDs are shorter within reserves (where risk is low) and that fish that spill over into the fished area take time to increase their FIDs. These findings imply that the presence of a marine reserve is even more beneficial to a fishery than previously expected — not only do fish spill over, but also those that do are naive and more easily caught. Marine-reserve advocates will be delighted by this suggestion.

Are these results surprising, and are they important? Yes, and yes. I suspect that they will surprise those fishery scientists who use catch statistics as their primary data, and who tend to think of fish as hanging around waiting to be caught, although they will not surprise biologists who watch fish before the fish are caught. Fish are behaving beings, and are highly capable of adapting their behaviour to particular circumstances. Their behaviour as larvae, for example, gives them amazing control over their dispersal8, and, as juveniles and adults, behaviour adds much of the complexity that builds up fish social structures and contributes to the challenges of managing some fisheries. Januchowski-Hartley and colleagues' results are a direct demonstration of an unexpected consequence of adaptive fish behaviour, and they will be relevant to anyone seeking to quantify the effects of a marine reserve on fishery yields.

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Correspondence to Peter F. Sale.

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Sale, P. Older but less wise. Nature 493, 167–168 (2013). https://doi.org/10.1038/493167a

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