Biogenic marine habitats are increasingly threatened by a multitude of human impacts, and temperate coasts in particular are exposed to progressively more intense and frequent anthropogenic stressors. In this study, the single and multiple effects of the urban stressors of nutrification and sedimentation on kelp bed communities were examined within Australia’s largest urbanised embayment (Port Phillip Bay, Victoria). Within this system, grazing by sea urchins (Heliocidaris erythrogramma) plays an important role in structuring reef communities by overgrazing kelp beds and maintaining an alternative and stable urchin barrens state. It is therefore important to explore the effects of urban stressors on kelp bed dynamics related to urchin abundance, and test the relative strengths of bottom-up and / or physical drivers (e.g. elevated nutrients and sediment) versus top-down (e.g. urchin grazing) forces on kelp bed community structure. The interactions of these drivers were assessed to determine whether their combination has synergistic, antagonistic, or additive effects on kelp beds. It was found that kelp responds positively to nutrient enhancement, but when combined with enhanced abundance of grazing sea urchins, the local positive effect of nutrient enhancement is overwhelmed by the negative effect of increased herbivory. Turf-forming algae behaved very differently, showing no detectable response to nutrification, yet showing a positive response to urchins, apparently mediated by overgrazing of canopy-forming algae that limit turf development. No direct effects of enhanced sediment load (at twice the ambient load) were found on intact kelp beds. Collectively, the results demonstrate that the ‘top-down’ control of urchin grazing locally overwhelms the positive ‘bottom-up’ effect of nutrient enhancement, and that intact kelp beds demonstrate resilience to direct impacts of urban stressors.

Sea urchins have the capacity to destructively overgraze kelp beds and cause a wholesale shift to an alternative and stable ‘urchin barren’ state. However, their destructive grazing behaviour can be highly labile and contingent on behavioural shifts at the individual and local population level. Changes in supply of allochthonous food sources, i.e. availability of drift-kelp, is often suggested as a proximate trigger of change in sea urchin grazing behaviour, yet field tests of this hypothesis are rare. Here we conduct a suite of in situ behavioural surveys and manipulative experiments within kelp beds and on urchin barrens to examine foraging movements and evidence for a behavioural switch to an overgrazing mode by the Australian sea urchin Heliocidaris erythrogramma (Echinometridae). Tracking of urchins using time-lapse photography revealed urchin foraging to broadly conform to a random-walk-model within both kelp beds and on barren grounds, while at the individual level there was a tendency towards local ‘homing’ to proximate crevices. However, consistent with locally observed ‘mobile feeding fronts’ that can develop at the barrens-kelp interface, urchins were experimentally inducible to show directional movement toward newly available kelp. Furthermore, field assays revealed urchin grazing rates to be high on both simulated drift-kelp and attached kelp thalli on barren grounds, however drift-kelp but not attached kelp was consumed at high rates within kelp beds. Time-lapse tracking of urchin foraging before/ after the controlled addition of drift-kelp on barrens revealed a reduction in foraging movement across the reef surface when drift-kelp was captured. Collectively results indicate that the availability of drift-kelp is a pivotal trigger in determining urchin feeding modes, which is demonstrably passive and cryptic in the presence of a ready supply of drift-kelp. Recovery of kelp beds therefore appears possible if a sustained influx of drift-kelp was to inundate urchin barrens, particularly on reefs where local urchin densities and where grazing pressure is close to the threshold enabling kelp bed recovery.

Shifts from productive kelp beds to impoverished sea urchin barrens occur globally and represent a wholesale change to the ecology of sub-tidal temperate reefs. Although the theory of shifts between alternative stable states is well advanced, there are few field studies detailing the dynamics of these kinds of transitions. In this study, sea urchin herbivory (a ‘top-down’ driver of ecosystems) was manipulated over 12 months to estimate (1) the sea urchin density at which kelp beds collapse to sea urchin barrens, and (2) the minimum sea urchin density required to maintain urchin barrens on experimental reefs in the urbanised Port Phillip Bay, Australia. In parallel, the role of one of the ‘bottom-up’ drivers of ecosystem structure was examined by (3) manipulating local nutrient levels and thus attempting to alter primary production on the experimental reefs. It was found that densities of 8 or more urchins m-2 (≥ 427 g m-2 biomass) lead to complete overgrazing of kelp beds while kelp bed recovery occurred when densities were reduced to ≤ 4 urchins m-2 (≤ 213 g m-2 biomass). This experiment provided further insight into the dynamics of transition between urchin barrens and kelp beds by exploring possible tipping-points which in this system can be found between 4 and 8 urchins m-2 (213 and 427 g m-2 respectively). Local enhancement of nutrient loading did not change the urchin density required for overgrazing or kelp bed recovery, as algal growth was not affected by nutrient enhancement.