Forming Sea Urchin Barrens from the Inside Out: an Alternative Pattern of Overgrazing

Vol. 464: 179–194, 2012 MARINE ECOLOGY PROGRESS SERIES Published September 19 doi: 10.3354/meps09881 Mar Ecol Prog Ser OPENPEN ACCESSCCESS Forming sea urchin barrens from the inside out: an alternative pattern of overgrazing E. B. Flukes*, C. R. Johnson, S. D. Ling Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 129, Hobart, Tasmania 7001, Australia ABSTRACT: Overgrazing by sea urchins on temperate reefs can affect a phase shift from macro - algal 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 time- lapse 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. 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 INTRODUCTION that triggers a shift from dense macroalgal beds to ‘barrens’ habitat largely devoid of fleshy macroalgae Marine ecosystems worldwide are subject to in - (e.g. Lawrence 1975, Bernstein & Mann 1982, creasing anthropogenic stress, lowering their Harrold & Reed 1985, Andrew & Underwood 1989, resilience to ‘catastrophic shifts’ (after Scheffer et al. Johnson et al. 2005, 2011). Sea urchin barrens are 2001) in ecological structure and function (Beisner et characterised by decreased habitat complexity, bio- al. 2003). Grazing by herbivores is frequently impli- diversity and productivity relative to adjacent sea- cated as a driver of phase shifts in marine environ- weed beds (Chapman 1981, Himmelman et al. 1983, ments via the removal of primary producers and bio- Tuya et al. 2005, Ling 2008). Unlike terrestrial herbi- genic habitat. In shallow temperate waters, sea vores that frequently overgraze their food, sea urchins are one of the most dominant and conspicu- urchins are capable of maintaining high density ous habitat-structuring taxa on rocky reefs, particu- populations on barrens by switching to alternative larly through their propensity for intensive grazing food sources including microalgae, non-geniculate *Email: [email protected] © Inter-Research 2012 · www.int-res.com 180 Mar Ecol Prog Ser 464: 179–194, 2012 coralline algae, drift algae (Johnson et al. 1981) and and persistent barrens habitat across ~50% of all invertebrate material (Ling 2008). The transition to near-shore rocky reef (Andrew & O’Neill 2000). In barrens habitat is particularly problematic because it recent decades, the species has extended its range represents a catastrophic phase shift between alter- southward to Tasmania, driven primarily by native stable states with hysteresis (e.g. Ling et al. increased poleward penetration of the East Aus- 2009a), requiring extensive reductions in sea urchin tralian Current (Johnson et al. 2005, Ling et al. densities for kelp beds to recover (Harrold & Reed 2009b), and the establishment of reproductively 1985, Carpenter 1990). viable populations in Tasmanian waters has further Few studies have employed an experimental facilitated its spread and establishment (Johnson et approach to elucidate the mechanism of grazing al. 2005, Ling et al. 2008, Banks et al. 2010). Wide- dynamics leading to the creation of barrens habitat. spread barrens are now found extensively in the Among these, most have focussed on species of sea northeast of Tasmania, with a gradient of decreasing urchins in the family Strongylocentrotidae (e.g. grazing intensity with latitude manifesting as patchy Mattison et al. 1977, Dean et al. 1984, Dumont et al. barrens decreasing in size and frequency down the 2007, Lauzon-Guay & Scheibling 2007b, Feehan et east coast of Tasmania (Johnson et al. 2005, 2011). al. 2012). This focus in research is due in part to the Continued barrens formation throughout the range- wide geographical distribution of strongylocentrotids extension region in Tasmania poses a major threat to and their close proximity to northern hemisphere local biodiversity (Ling 2008) and to the lucrative researchers, in combination with a spectacular and reef-based abalone and rock lobster fisheries depen- highly conspicuous mode of overgrazing that in - dent on macroalgal production and habitat (Johnson volves the formation of 3-dimensional ‘feeding fronts’ et al. 2011). Importantly, removal of predatory spiny at the interface between kelp bed and barren habi- lobsters from Tasmanian rocky reefs via commercial tat. Manifestation of this phenomenon appears to and recreational fishing has reduced the resilience of coincide with a switch in behaviour from low-effect kelp beds, increasing the risk of catastrophic shift to sedentary or cryptic foraging to destructive motile widespread barren habitat (Ling et al. 2009a). and exposed feeding aggregations (e.g. Harrold & In common with other diadematid sea urchins Reed 1985). The likelihood of barrens formation is (Nelson & Vance 1979, Lissner 1980, 1983), divers therefore usually associated with complex behaviour observe Centrostephanus rodgersii to shelter in involving threshold densities, and this pattern has crevices during the day and emerge to forage at been widely accepted and generalised across sea night (reviewed by Andrew & Byrne 2001). In Tasma- urchin taxa (e.g. Mattison et al. 1977, Dean et al. nia, C. rodgersii within dense macroalgal beds graze 1984, Lauzon-Guay & Scheibling 2007a). Our casual discrete patches surrounding their crevices to form observations over several thousand person-hours of local barren patches, termed ‘incipient barrens’ diving across hundreds of kilometres of coastline in (Johnson et al. 2005). Formation of widespread bar- Tasmania indicate that Centrostephanus rodgersii rens occurs more frequently on boulder substratum does not form grazing fronts in creating extensive sea where localised shelters are abundant, although bar- urchin barrens, but this species forms relatively small rens may also form on featureless flat-rock substrata patches which can eventually be come sufficiently (Johnson et al. 2005, Ling & Johnson 2012), which numerous to grow, coalesce and form extensive areas sea urchins will graze from nearby rudimentary of barrens habitat. In the present paper, we identify ‘shelter’ when all available crevices are occupied or behaviour consistent with our general observation of persist exposed on flat rock surfaces throughout the forming barrens habitat from the ‘inside out’ without entire diel cycle (e.g. Andrew & O’Neill 2000). The the formation of grazing fronts. These findings indi- availability of crevice structure has been shown to cate that well-established models of barrens forma- mitigate the vulnerability of C. rodgersii to predation tion do not apply universally across all systems and (Ling & Johnson 2012), with such crevice depen- sea urchin taxa. dency found to influence the sea urchins grazing The role played by the diadematid sea urchin patterns to the extent that Andrew (1993) suggested Centrostephanus rodgersii in structuring shallow that availability of crevices for shelter within kelp rocky reef communities is unparalleled by any other beds is a pre-requisite condition for barren forma- benthic herbivore in southeastern Australia (re- tion. Thus, the development from incipient through viewed by Andrew & Byrne 2001, Johnson et al. extensive barrens on boulder substratum and finally 2005, 2011). Throughout the species’ historical range to widespread barrens habitat on extensive areas of in New South Wales (NSW), it maintains widespread flat rock represents an increasing gradient of forag- Flukes et al.: An alternative model of urchin overgrazing 181 ing intensity that is effectively spatially mapped range-extension region (Fig. 1). Each monitored reef along the urchin’s recent range-extension region in was characterised by moderate topographic relief eastern Tasmania. The prevalence of incipient reaching a maximum depth of 12 to 16 m, with a barrens on this coast therefore represents a crucial macroalgal

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