Decadal trends in marine reserves reveal differential rates of change in direct and indirect effects

Abstract

Decadal-scale observations of marine reserves suggest that indirect effects on taxa that occur through cascading trophic interactions take longer to develop than direct effects on target species. Combining and analyzing a unique set of long-term time series of ecologic data in and out of fisheries closures from disparate regions, we found that the time to initial detection of direct effects on target species (±SE) was 5.13 ± 1.9 years, whereas initial detection of indirect effects on other taxa, which were often trait mediated, took significantly longer (13.1 ± 2.0 years). Most target species showed initial direct effects, but their trajectories over time were highly variable. Many target species continued to increase, some leveled off, and others decreased. Decreases were due to natural fluctuations, fishing impacts from outside reserves, or indirect effects from target species at higher trophic levels. The average duration of stable periods for direct effects was 6.2 ± 1.2 years, even in studies of more than 15 years. For indirect effects, stable periods averaged 9.1 ± 1.6 years, although this was not significantly different from direct effects. Populations of directly targeted species were more stable in reserves than in fished areas, suggesting increased ecologic resilience. This is an important benefit of marine reserves with respect to their function as a tool for conservation and restoration.

Fig. 1.

Long-term changes in key populations at temperate no-take marine reserve locations and reference (fished) areas. Data are means (±SE), expressed as a ratio of the observed (t = x) vs. initial values at the time reserves were implemented (t = 0) and were log transformed for presentation and comparison. Temperate species: Leigh; lobster Jasus edwardsii, snapper Pagrus auratus, urchin Evechinus chloroticus, and kelp Ecklonia radiata. Maria; lobster J. edwardsii, predatory fish (species complex >300 mm fork length and excluding highly mobile species), urchin Heliocidaris erythrogramma, abalone Haliotis rubrum, and macroalgal canopy cover (species complex of large brown algae). Anacapa; lobster Panulirus interruptus, sheephead Semicossyphus pulcher, urchin Strongylocentrotus purpuratus, and kelp (Laminarian species complex). All values based on density estimates except for kelp canopy at Maria Island (percentage).

Fig. 2.

Long-term changes in key populations at tropical no-take marine reserve locations and reference (fished) areas. Data are means (±SE), expressed as a ratio of the observed (t = x) vs. initial values at the time reserves were implemented (t = 0) and were log transformed for presentation and comparison. Tropical species: Sumilon; large predators Serranidae and Lutjanidae, omnivore Hemigymnus melapterus, herbivore Scarus tricolor. Apo; large predators Serranidae and Lutjanidae, omnivore Hemigymnus melapterus, herbivore Scarus tricolor, planktivore Naso vlamingi. Kenya; large predators including triggerfish Balistidae and wrasses, herbivores (species complex), and urchin Echinometra mathaei. All values based on density estimates, except for Kenyan case study, in which biomass (fish and urchins) and percentage cover (corals and algae) are used.

Fig. 3.

Time to first detection of direct and indirect responses to marine reserve protection. Positive data indicate the proportion of observed species displaying direct and indirect effects, negative values indicate taxa for which no effect was observed. n = 28.