Experimental demonstration of a trophic cascade in the Galápagos rocky subtidal: Effects of consumer identity and behavior

Abstract

In diverse tropical webs, trophic cascades are presumed to be rare, as species interactions may dampen top-down control and reduce their prevalence. To test this hypothesis, we used an open experimental design in the Galápagos rocky subtidal that enabled a diverse guild of fish species, in the presence of each other and top predators (sea lions and sharks), to attack two species of sea urchins grazing on benthic algae. Time-lapse photography of experiments on natural and experimental substrates revealed strong species identity effects: only two predator species-blunthead triggerfish (Pseudobalistes naufragium) and finescale triggerfish (Balistes polylepis)-drove a diurnal trophic cascade extending to algae, and they preferred large pencil urchins (Eucidaris galapagensis) over green urchins (Lytechinus semituberculatus). Triggerfish predation effects were strong, causing a 24-fold reduction of pencil urchin densities during the initial 21 hours of a trophic cascade experiment. A trophic cascade was demonstrated for pencil urchins, but not for green urchins, by significantly higher percent cover of urchin-grazed algae in cages that excluded predatory fish than in predator access (fence) treatments. Pencil urchins were more abundant at night when triggerfish were absent, suggesting that this species persists by exploiting a nocturnal predation refuge. Time-series of pencil urchin survivorship further demonstrated per capita interference effects of hogfish and top predators. These interference effects respectively weakened and extended the trophic cascade to a fourth trophic level through behavioral modifications of the triggerfish-urchin interaction. We conclude that interference behaviors capable of modifying interaction strength warrant greater attention as mechanisms for altering top-down control, particularly in speciose food webs.

Fig 1

(A) Green (Lytechinus semituberculatus) and pencil (Eucidaris galapagensis) sea urchins on the exposed rocky substrate, 8 m depth, Galápagos Islands and (B) close-up of a patch of substrate on the bases grazed by pencil urchins in the TC experiment. Pink areas are crustose coralline algae which is consumed by both species. Orange organisms are an ahermatypic coral Tubastrea sp. Scale bar in (B) is 2.0 cm. The grazed area is a light-colored crescent shaped patch approximately 2.0–3.0 cm wide extending across the upper half of the photograph. These areas were measured as a percent of the substrate grazed by sea urchins in the TC experiments. Also shown are crustose coralline algae (pink), fleshy encrusting algae Hildenbrandia sp. (brown), green algal turf, and diatoms (light brown).

Fig 2

(A-B) Pencil urchin (Eucidaris) survivorship and prey selection from tethering experiments. Data points represent the number of surviving small urchins at 1 minute intervals in A-B, and the number of large urchins surviving at 2 min. intervals in C., all from time-lapse photographs. Gray bars below the x-axis in B and C represent night time hours of darkness. Experiments in A were conducted at Rocas Gordon on May 18, 2007 and at Baltra South on May 22 and May 23, 2007, and in B at Isla Champion (January 11, 2008, open triangles) and Rocas Gordon (January 7, 2008 open circles). (C) Survivorship from trials where blunthead and finescale triggerfish consumed the large urchins. The diamond symbols represent a trial initiated on June 27, 2008 while the circles represent a trial begun on July 3, 2008. (D) Average urchin survivorship from two trials of prey selection experiments performed with tethered green urchins (open diamond and triangles) and pencil urchins (black diamond and triangles) placed next to each other on the substrate.

Fig 3. Diel patterns of pencil urchin density at the Baltra South site.

Data represent the number of urchins per 1.3 m ² on the exposed substrate as determined by counting urchins in time-lapse photographs in 2 trials beginning on June 27 and on July 3, 2008. The grey bar below the x axis represents night hours. Note the rapid increase in urchin abundance during the early hours of night and that urchins are exposed on the substrate during the day.

Fig 4

Results of the trophic cascade experiments with pencil urchin (A) and green sea urchin prey (B). Bars represent the average percent (+/- SE) of algal covered substrate grazed by urchins in 8 days (A) and 7 days (B). Note that no algae was grazed by pencil urchins in the treatments accessible to predatory fish because they were eaten by triggerfish, providing evidence of a tri-trophic cascade. Green urchins were unregulated by predation and consumed large amounts of algae (B). No algae was lost in the controls (not shown) indicating that environmental factors did not influence the treatment results. (C) Photo from the time-lapse record showing a blunthead triggerfish attacking a pencil urchin during the TC experiment in a fence (predator access) treatment on the morning of June 24, 2012. A caged control is shown to the left of the fence treatment.

Fig 5

(A) Observed and model-fit pencil urchin survivorship during the initial 20.5 hours of the TC experiment and (B) consumer co-occurrences during initial 21 hours of the 8 day pencil urchin TC experiment (11:46 until ~ 09:00 the next morning) when blunthead and finescale triggerfish were present. All of the exposed urchins in the predator access treatments were eaten by blunthead triggerfish (Fig 4C). Inset graph shows the same survivorship results plotted on a logarithmic scale to show the occurrence of triggerfish, hogfish and top-predators (sharks and sea lions). (B) Data points represent the first time point that a species was observed in the time-lapse record (entrance time in seconds, y axis) as an indicator of consumer species overlap. Actual consumer residence times are presented in Table 2. Predator images below the x-axis represent hogfish, blunthead triggerfish, finescale triggerfish, Galápagos sharks, hammerhead shark, sea lions, yellow bellied triggerfish, green turtles, and white tip sharks (from left to right).

Fig 6. Summary of the density- and behaviorally-mediated interactions characterizing the inferred mechanisms of top-down control in the Galápagos rocky subtidal.

Black arrows represent negative interactions with the line thickness roughly proportional to the strength of the interaction. Gray arrows represent a result of the model fitted to pencil urchin survivorship in the TC experiment to quantify hogfish and top-predator interference rates. Dashed lines represent inferred indirect effects. The model parameter a represents the per capita attack rate of triggerfish on urchins. Parameters b and c respectively represent the interference rates with which hogfish and top-predators (sharks and sea lions) affected the strength of the triggerfish-urchin interaction. Parameter g represents the per capita grazing rates of the two urchin species. See S4 Table for more information.