Current empirical evidence overwhelmingly supports the theory that foraging–risk trade-offs should result in predator presence weakening per capita
impacts of grazers on plants in three-level food chains (reviewed by Schmitz et al.
]). On the contrary, our field observations and subsequent experimentation in a salt marsh revealed that the non-consumptive effects of top predators can act to strengthen the per capita
impacts of grazing snails on Spartina
—the vascular plant that forms vast monocultures in this highly productive and valuable intertidal ecosystem.
Our results indicate that the negative effect of top predators on Spartina
was driven by the vertical habitat shift undertaken by Littoraria
(), which in turn increased the per capita
impacts of this grazer on leaves and overall plant biomass ().The predator-induced habitat shift of Littoraria
probably reflects a trade-off between the multiple benefits of remaining close to the substrate (e.g. minimal investment in climbing activity, reduced risk from avian predators and proximity to energy-rich substrate microalgae) and the risk of predation from substrate-dwelling predators. The vertical habitat shift of Littoraria
can be further explained in terms of both predator foraging mode, and predator and prey habitat domains [5
]. Firstly, the sit-and-wait predatory crabs provide spatially consistent point source cues, and are thus potentially effectively avoided by prey. Secondly, the broad vertical habitat domain of Littoraria
relative to its predators allowed it to respond to these spatially consistent cues, reducing predation risk with a chronic shift in foraging activity from the risky benthos and lower Spartina
stems, to the canopy of Spartina
plants, beyond the reach of ground-dwelling predatory crabs. Thus, the perpendicular orientation of risk (horizontal, across the substrate) and refuge (vertical, away from the substrate) habitats predictably drove grazers vertically (), to the vulnerable and important canopy leaves of Spartina
, and consequently strengthened the negative per capita
grazer–plant interactions ().
Although this study is the first experimental demonstration of a negative TMII generated by contrasting predator (horizontal) and prey (vertical) habitat domains, we predict that similar, but yet undetected, effects may occur in many other systems because of how common this perpendicular movement contrast is in nature. For example, across temperate and tropical forests and in savannahs with dotted tree cover, facultatively leaf-eating prey (e.g. baboons, other monkeys, small mammals) often find refuge from ground-dwelling predators (lions, hyenas, canines) by climbing up trees [1
]. Similarly, in mangroves and kelp beds around the world, snails are thought to maintain high climbing heights in the canopies of dominant plants to reduce predation by substrate-bound carnivores (e.g. crabs, lobsters [12
By experimentally preventing prey capture, we revealed a negative TMII between predators and plants in our study system. Under natural field conditions however, these predators also consume Littoraria
, and many exert substantial control on their densities [9
]. This system thus probably exhibits opposing trait-mediated (negative) and density-mediated (positive) indirect interactions between top predators and plants, with the net effect of predators being determined by the relative strengths of these indirect interactions. Notably, while we focus here on the negative TMII between predators and the biomass of the single habitat-forming vascular plant species in this system (Spartina
), future studies must additionally quantify the potentially positive effect of Littoraria's
habitat shift on substrate microalgae to ascertain the sign of the TMII on the overall community primary production.
Despite the bewildering complexity of species interactions, non-consumptive effects of top predators on herbivores may be explained (and ultimately predicted) in terms of simple, universal traits—hunting mode of the top predators and the relative orientation of the habitat domains of both top predator and herbivores (this study [5
]). This information, combined with explicit consideration of the functional importance of resources in refuge habitats, probably explains our findings and provides a powerful tool to predict the direction of trait-mediated indirect effects of predators in other important ecosystems dominated by three-dimensional, canopy-generating plants.