Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift

Abstract

A key consideration in assessing impacts of climate change is the possibility of synergistic effects with other human-induced stressors. In the ocean realm, climate change and overfishing pose two of the greatest challenges to the structure and functioning of marine ecosystems. In eastern Tasmania, temperate coastal waters are warming at approximately four times the global ocean warming average, representing the fastest rate of warming in the Southern Hemisphere. This has driven range extension of the ecologically important long-spined sea urchin (Centrostephanus rodgersii), which has now commenced catastrophic overgrazing of productive Tasmanian kelp beds leading to loss of biodiversity and important rocky reef ecosystem services. Coincident with the overgrazing is heavy fishing of reef-based predators including the spiny lobster Jasus edwardsii. By conducting experiments inside and outside Marine Protected Areas we show that fishing, by removing large predatory lobsters, has reduced the resilience of kelp beds against the climate-driven threat of the sea urchin and thus increased risk of catastrophic shift to widespread sea urchin barrens. This shows that interactions between multiple human-induced stressors can exacerbate nonlinear responses of ecosystems to climate change and limit the adaptive capacity of these systems. Management actions focused on reducing the risk of catastrophic phase shift in ecosystems are particularly urgent in the face of ongoing warming and unprecedented levels of predator removal from the world's oceans.

Fig. 1.

Recent climate-driven range extension of the long-spined sea urchin to eastern Tasmania. (A) Sea surface temperature (SST) map of south eastern Australia showing influence of the warm East Australian Current in eastern Tasmania during Austral winter; data are mean SST (Pathfinder, 4 × 4 km pixels) for June–August 1993–2007. Dates show year of first observations of Centrostephanus rodgersii at sites on the Tasmanian coast. (B) Long-term winter warming trend of coastal waters in eastern Tasmania 1950–2008; data are 4 year running means (see Materials and Methods) for August, the month of major C. rodgersii spawning (15); dashed line indicates the lower temperature limit for the development of C. rodgersii larvae (15); inset shows 21-day-old C. rodgersii echinopluteus.

Fig. 2.

Catastrophic shift between kelp beds and sea urchin barrens. (A) Conceptual schematic of discontinuous phase shift (redrawn from ref. 3). If the reef system occurs in the kelp state on the upper path (red) but close to the threshold F₁, a slight increase in sea urchin density may induce a catastrophic “forward-shift” to the alternative and stable sea urchin barrens state. Once barrens have formed, reverting back to the kelp state is difficult because the system demonstrates hysteresis (18), and the “reverse-shift” (blue path) occurs only if sea urchin density is reduced below the return threshold at F₂. The broken gray line indicates the region of instability between the alternative stable states. (B) Macroalgal cover versus Centrostephanus rodgersii density in eastern Tasmania. Bubble size represents relative frequency of particular urchin density and macroalgal cover combinations as measured in 575 individual 5 m² plots at 13 sites spanning the east coast (11). Overlaid arrows and numbers in parentheses indicate magnitude and direction of ecosystem response to removals and additions of C. rodgersii. Removals of C. rodgersii from barrens (blue arrows) in: NSW after 18 months (18, 19) where starting sea urchin densities were 10 and 6 m⁻² respectively; after approximately 5 months (20), with a starting sea urchin density of 4 m⁻²; in Tasmania after 18 months (12) with a starting sea urchin density of 2 m⁻². Additions of C. rodgersii to kelp beds (red arrows) in NSW after approximately 5 months (20), starting sea urchin density 0 m⁻². Dashed lines with arrows represent the theoretical “forward-shift” and “reverse-shift” paths as explained in (A).

Fig. 3.

(A) Size-specific predation by lobsters [Carapace Length (CL)] on long-spined sea urchins [Test Diameter (TD)] in eastern Tasmania. Successful predation events are indicated by filled circles obtained by in situ video monitoring (black circles) and aquarium trials (gray circles), open circles indicate lobster-urchin encounters but with no predation. The solid curve is the theoretical physical limit of predation (y = 5.12e^0.023x) determined by the capacity of a lobster to straddle a sea urchin and prise it from the substratum using its first pair of walking legs; LHS of plot is size-frequency of emergent Centrostephanus rodgersii on eastern Tasmanian reefs (n = 1972). As evidenced by the upper limit of observed predation events in situ (i.e., the ceiling of filled black circles, which here is given by the dashed curve fitted as 60% of upper theoretical limit), lobsters must be approximately >140 mm CL to be effective predators of emergent sea urchins in the wild. The minimum legal size-limits for this lobster in Tasmania are 105 mm CL for females and 110 mm CL for males, note that there is no maximum harvestable size-limit. (B) Population trajectories of tagged C. rodgersii on reefs inside and outside MPAs; data are mean percentages (± SEM) of populations surviving (initial population size was 96 individuals at each of two MPA and two fished sites). (C) Change in size-frequency of lobsters pre- (1960s) and post-intense fishing (1990s) in north eastern Tasmania showing pronounced fish-down of the size class CL greater than or equal to140 mm as revealed by fishery independent trap lifts, redrawn from (9).

Fig. 4.

Conceptualization of loss of kelp bed resilience because of fishing and associated increase in risk of catastrophic phase shift to the Centrostephanus rodgersii barrens state. Alternative basins of attraction represent kelp bed and sea urchin barrens states and the position of the ball represents ecosystem status. To shift to barrens habitat the kelp system must be perturbed sufficiently for the ball to roll from one basin to another (dashed arrow). (A) Prefished kelp bed with high abundance of large predatory lobsters and high resilience (indicated by basin depth). (B) Heavily fished kelp beds with shallow ‘basin’ and thus lower resilience. Solid arrows represent perturbation of the kelp bed state in the form of climate-driven incursion of C. rodgersii. The likelihood of catastrophic shift to sea urchin barrens depends on the size of the perturbation, which is the same in both (A) and (B), and the basin depth, i.e., “resilience stability” of the kelp-dominated state.