title: Shifts in intertidal zonation and refuge use by prey after mass mortalities of two predators.
abstract: Recent mass mortalities of two predatory sea star species provided an unprecedented opportunity to test the effect of predators on rocky intertidal prey. Mass mortalities provide insight that manipulative experiments cannot because they alter ecosystems on a larger scale, for longer time periods, and remove both organisms and their cues from the environment. We examined shifts in population size structure, vertical zonation, and use of emersed refuge habitats outside tidepools by the abundant herbivorous black turban snail Tegula funebralis, both before and after the successive mortalities of two predatory sea stars. The small cryptic predator Leptasterias spp. suffered a localized but extreme mortality event in November 2010, followed by two mass mortalities of the keystone predator Pisaster ochraceus in August 2011 and autumn 2013. After the local extinction of Leptasterias, the population size of Tegula more than doubled. Also, since Leptasterias primarily inhabited only mid to low intertidal tidepools at this site, small and medium sized snails (which are preferred by Leptasterias) shifted lower in the intertidal and into tidepools after the mortality of Leptasterias. After the mortality of Pisaster in August 2011, large snails did not shift lower in the intertidal zone despite being preferred by Pisaster. Small and medium sized snails became denser in the higher zone and outside tidepools, which was not likely due to Pisaster mortality. Previous studies concluded that Pisaster maintained vertical size gradients of snails, but our data implicate the overlooked predator Leptasterias as the primary cause. This natural experiment indicated that (1) predators exert top-down control over prey population sizes and lower limits, (2) vertical zonation of prey are dynamic and controlled in part by prey behavior, and (3) predators exert the strongest effects on more vulnerable individuals, which typically inhabit stressful habitats higher on the shore or outside tidepools to avoid predation. Because the mass mortalities of two predators drastically reduced both the predation pressure and the chemical cues of predators in the environment, we were able to investigate both the effects of predators on prey populations and the effects on mobile prey behavior.
authors.affiliation: Bodega Marine Laboratory, Environmental Science and Policy Department, University of California Davis, 2099 Westside Road, Bodega Bay, California, 94923, USA.
authors.forename: Sarah A
authors.identifier: http://orcid.org/0000-0002-3857-9930
authors.initials: SA
authors.lastname: Gravem
authors.affiliation: Bodega Marine Laboratory, Environmental Science and Policy Department, University of California Davis, 2099 Westside Road, Bodega Bay, California, 94923, USA.
authors.forename: Steven G
authors.initials: SG
authors.lastname: Morgan
mesh_terms: D000818:Animals; D017753:Ecosystem; D009026:Mortality; D011156:Population Density; D011235:Predatory Behavior; D012908:Snails / Q000502:physiology*; D013215:Starfish / Q000502:physiology*
keywords: 
  Pisaster ochraceus
  ; 
  Tegula funebralis
  ; Leptasterias spp.; intertidal zonation; mass mortality; natural experiment; nonconsumptive effects; sea star wasting disease; size-dependent predation; tidepool; top-down control; vertical size gradient