Indirect interactions in seagrasses: fish herbivores increase predation risk to sea urchins by modifying plant traits

Abstract

Summary 1.The dominant paradigm of top-down control of ecological communities through direct consumption pathways is giving way to a more nuanced understanding of trophic interactions with the recognition that subtler indirect effects can often play an important role in structuring communities. Direct and indirect trophic and non-trophic processes could well be acting simultaneously within the same food web, and their overall effects may even interact with each other. 2. We studied indirect interactions in a relatively simple trophic system comprising a single producer, two herbivores and a guild of predators. In particular, we assessed whether (i) the principal herbivore fish, Sarpa salpa, is capable of modifying a seagrass trait, canopy height, by grazing and (ii) whether grazing-induced habitat alteration can trigger an environment-mediated modification of the interaction between herbivorous sea urchins Paracentrotus lividus and their predators. 3. We tested these hypotheses with field experiments including fish herbivore-exclusion experiments (to examine the ability of S. salpa to modify seagrass habitats) and predation experiments using tethered sea urchins in a meadow with varying canopy heights (to test whether habitat modification can mediate urchin predation risk). 4. The effect of S. salpa herbivory was highly significant. Canopy height in herbivore-excluded plots was more than 3Á5 times higher than in uncaged control plots. In addition, adult sea urchin predation risk in the most highly grazed plots was 4-5 times higher than plots with higher canopy heights. In contrast, predation risk on juvenile urchins was not influenced by canopy height. 5. Our results show that predation pressure on a key herbivore can be modified both by the environmental context within which it finds itself and by the actions of another herbivore that modifies the plant traits that create this environmental context. These act as two discrete pathways that interact in potentially nonlinear ways, mediating top-down control in these ecosystems. Herbivores, particularly when acting as ecosystem engineers, may have the potential to mediate and increase predation risk, as they substantially modify habitat structure, with consequences for refuge availability, among others. Assessing these indirect interactions is not just important to understand the functioning of the system itself but may have important management and conservation consequences.

Age and size compositions, habitats, growth and reproductive characteristics of a terapontid (Pelates octolineatus) in coastal waters

“…Such a view is consistent with the fact that, in Shark Bay, over 800 km further north, P. octolineatus was the dominant grazer of seagrasses in the extensive meadows of a sub-tropical embayment, where this omnivore consumes whole blades and is considered likely to play a significant role in removing leaf tissue from the abundant seagrass species Halophila spinulosa (Burkholder et al 2012). This parallels the high levels of herbivory by Sarpa salpa in the Mediterranean Sea (Pagès et al 2012) and Leptoscarus vaigiensis in IndoPacific waters (Unsworth et al 2007), and the strong influence of these dominant grazers on the structure and function of their associated seagrass ecosystems. One of the most striking features of P. octolineatus on the lower western Australian coast is its marked seasonal pattern of growth, presumably reflecting the limited period in which water temperatures are conducive to growth.…”

Herbivory on freshwater and marine macrophytes: A review and perspective

“…Fish productivity was found to be lower in seagrass meadows grazed by green turtles (Arthur et al, 2013) and after meadow collapse caused by overgrazing (reported for turtles in (Christianen et al, 2013). Similarly, herbivorous fishes, dugongs, geese and other waterbirds have been found to drastically reduce invertebrate biomass in seagrass meadows and salt marshes (Marklund et al, 2002;Sherfy and Kirkpatrick, 2003;Skilleter et al, 2007;Pages et al, 2012) . Impacts on invertebrates may occur even where the proportional reduction of vegetation is low (Bortolus et al, 1998).…”

Relating trophic resources to community structure: a predictive index of food availability

“…However, relatively little of this biomass is directly consumed by grazers, owing to various deterrent compounds [38,39]. Only a few herbivores, sometimes reaching high densities, are able to consume the abundant green leaf biomass, most notably sea urchins [40], some isopods [41] and a few fishes [42]. As predicted, modelled food availability does not necessarily correspond to food consumption.…”