Forming sea urchin barrens from the inside out: an alternative pattern of overgrazing

Abstract

Overgrazing by sea urchins on temperate reefs can affect a phase shift from macroalgal beds to 'barrens' habitat largely devoid of seaweeds. Existing models of barrens formation are derived largely from observations of strongylocentrotid urchins, which typically show a behavioural shift from cryptic feeding to exposed grazing fronts that move through and 'mow down' macroalgal beds. Foraging by the temperate diadematid urchin Centrostephanus rodgersii triggers a similar transition from intact macroalgal bed to widespread barren grounds but does not appear to involve a behavioural shift. Fine-scale foraging movements were observed using timelapse photography across the urchin's range-extension region and described with respect to a random walk model. Foraging was highly nocturnal, with individuals homing strongly to available crevices. In situ monitoring of tagged individuals suggests strong fidelity to and thus high stability of barren patches, while similar behavioural patterns across habitat types representing a gradient of foraging intensities indicate no behavioural shift associated with overgrazing. Laboratory experiments showed that C. rodgersii lacks a directional chemosensory response to either macroalgae or conspecifics. Combined evidence suggests a model of barrens formation fundamentally different to the well-established 'feeding front' model, with formation of widespread barrens by C. rodgersii occurring from the 'inside out' via growth and coalescence of small barrens patches that form within macroalgal beds as a result of additive localised grazing radiating from crevice shelters. Regulation of urchin density at the spatial scale of individual barrens patches is proposed as a viable option to manage the formation of widespread barrens habitat within the urchin's recent range-extension to eastern Tasmania. 464: 179-194, 2012 coralline algae, drift algae (Johnson et al. 1981) and invertebrate material (Ling 2008). The transition to barrens habitat is particularly problematic because it represents a catastrophic phase shift between alternative stable states with hysteresis (e.g. Ling et al. 2009a), requiring extensive reductions in sea urchin densities for kelp beds to recover (Harrold & Reed 1985, Carpenter 1990. KEY WORDS: Phase shift · Kelp beds · Barrens · Centrostephanus rodgersii · Foraging ecology · Movement · Grazing effect · Range extension Resale or republication not permitted without written consent of the publisher OPEN PEN ACCESS CCESSMar Ecol Prog SerFew studies have employed an experimental approach to elucidate the mechanism of grazing dynamics leading to the creation of barrens habitat. Among these, most have focussed on species of sea urchins in the family Strongylocentrotidae (e.g. Mattison et al. 1977, Dean et al. 1984, Dumont et al. 2007, Lauzon-Guay & Scheibling 2007b, Feehan et al. 2012). This focus in research is due in part to the wide geographical distribution of strongylocentrotids and their close proximity to northern hemisphere researchers, in combination with ...

Role of two co-occurring Mediterranean sea urchins in the formation of barren from Cystoseira canopy

“…This is due to the fact that sea urchin grazing is frequently responsible for the destruction of canopy-forming algae and the formation of barrens in shallow marine ecosystems (Lawrence, 2013 and references therein). Several studies have indicated a spatio-temporal variability of feeding behaviors (Konar and Estes, 2003;Flukes et al, 2012) and there is evidence that this may depend on local threshold density (Bulleri, 2013).…”

Successional patterns of hard-bottom macrobenthic communities at kelp bed (Lessonia trabeculata) and barren ground sublittoral systems

“…Kelp beds are very important because they provide habitat complexity, food resources and shelter, thus harbouring high levels of biodiversity compared with their barren ground counterparts (Dayton, 1985;Graham, 2004;Villegas et al, 2008). In contrast, barren grounds appear to flourish when kelp beds decay (Steneck et al, 2002;Flukes et al, 2012) and are principally dominated by crustose coralline algae and sea urchin species (Chapman, 1981).…”

Global regime shift dynamics of catastrophic sea urchin overgrazing

“…(a) state-dependent feedbacks reinforcing resilience (b) state-dependent stressors decreasing resilience macroalgal beds reference macroalgal beds to urchin barrens reference reference presence of functional urchin predators -macro-predators [4,9,[34][35][36][37][38] -micro-predators [39] *overharvesting of urchin predators [4,9,[34][35][36]38] multi-trophic consequences of prey-switching by natural predators [62] *presence of human urchin harvest/urchin culling [40] (*)presence of urchin disease [28] high macroalgal productivity -local standing macroalgae [29] -distant allocthonous inputs [41,42] large macroalgal bed biomass (patch-size dynamics) [16,19,43] propagule supply (connectivity) [4,44] natural barriers to urchin movement -high swell/ current exposure [45] -macroalgal whiplash [16,46] *kelp disease/overgrowth by inva sive algae/epiphytes [28,61] *direct removal of kelp -human harvest [63] (*)acute physical change -storms/ extreme weather [63] -warm periods promoting sea urchin larval survival [64] -cool periods promoting sea urchin recruitment [65] (*)chronic physical change -declining algal productivity due change in oceanography/ catchment processes [63,66] -declining algal productivity of allochthonous macroalgal 'drift' supply [67] -range-extension of urchins [10,…”

“…In Australia, no other benthic herbivore has had as large a role as C. rodgersii in determining the state of shallow reef communities [12,21], with thousands of kilometres of reef overgrazed within the historical range of the urchin across the New South Wales coast [22]. While widespread urchin barrens (100 000s m 2 ) are evident at several eastern Tasmanian reefs, smaller 'incipient barrens' (10s m 2 ) within otherwise intact kelp beds are common and considered an early warning sign of broader-scale kelp bed collapse along this coast [7,19].…”

“…This new manifestation of overgrazing has had clear negative impacts on commercial reef-based fisheries and local biodiversity [6][7][8]18], motivating the need to understand the dynamics of urchin grazing and the resilience of kelp beds to this threat [9,19,20]. In Australia, no other benthic herbivore has had as large a role as C. rodgersii in determining the state of shallow reef communities [12,21], with thousands of kilometres of reef overgrazed within the historical range of the urchin across the New South Wales coast [22].…”