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Fish-seastar facilitation leads to algal forest restoration on protected rocky reefs.
Galasso NM
,
Bonaviri C
,
Di Trapani F
,
Picciotto M
,
Gianguzza P
,
Agnetta D
,
Badalamenti F
.
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Although protected areas can lead to recovery of overharvested species, it is much less clear whether the return of certain predator species or a diversity of predator species can lead to re-establishment of important top-down forces that regulate whole ecosystems. Here we report that the algal recovery in a Mediterranean Marine Protected Area did not derive from the increase in the traditional strong predators, but rather from the establishment of a previously unknown interaction between the thermophilic fish Thalassoma pavo and the seastar Marthasterias glacialis. The interaction resulted in elevated predation rates on sea urchins responsible for algal overgrazing. Manipulative experiments and field observations revealed that the proximity of the seastars triggered an escape response in sea urchins, extending their tube feet. Fishes exploited this behavior by feeding on the exposed tube feet, thus impairing urchin movement, and making them vulnerable to predation by the seastars. These findings suggest that predator diversity generated by MPA establishment can activate positive interactions among predators, with subsequent restoration of the ecosystem structure and function through cascading consumer impacts.
Figure 1. Conceptual model of trophic interactions and their effect on habitat state in Mediterranean rocky reefs.(A) Interactions among the seastar M. glacialis, the ornate wrasse T. pavo, the sea urchins P. lividus and A. lixula and the algae Cystoseira spp. Dotted arrows indicate indirect interactions, whereas solid arrows indicate direct interactions. +/â symbols indicate positive or negative effect of the interaction on the species pointed by the arrow. In Ustica Island the interaction between fish and seastar (1) facilitates predation on sea urchins (2) by the seastar. Urchins are in turn strong grazers and are able to alter algal coverage (3). (B) Temporal trends in M. glacialis densities, sea urchin densities and habitat state in Ustica Island MPA. Red line: P. lividus. Black line: A. lixula. Blue bars: M. glacialis. Green line: algal coverage. Images in figure by F. Di Trapani and P. Gianguzza.
Figure 2. Attack speed (M. glacialis) and escape speed (P. lividus and A. lixula) measured in intact individuals (normal), control and treated individuals (with 50% and 70% tube feet removed) in forest (green bars) and barren (empty bars).A 3-way ANOVA was performed and significant effect of the term âTreatment X Habitatâ was found (Table 1). SNK a posteriori tests were run to investigate the differences found (Table 1); similar letters (a, b, c, d) indicate groups of data not significantly different. In forest, M. glacialis was faster than P. lividus and A. lixula (normal, intact, control and treated). In barren, M. glacialis was faster than P. lividus and A. lixula when 70% and 50% tube feet, respectively, were removed (Table 1). We observed that M. glacialis is able to âfloatâ above the forest thanks to its long arms, while urchin movement was affected by their spines tangling among the thalli of erect algae (Table 1).
Figure 3. Simulation of the effect of tube feet removal on escape velocity and predation outcome on the barren habitat based on experimental data (Table 1, Fig. 2).Vâ=âMean velocity (±s.e.). of attacking M. glacialis and escaping sea urchins (A. lixula and P. lividus). Removal of 70% and 50% of tube feet respectively in P. lividus and A. lixula allows the predator M. glacialis to reach and consume them. Simulated reaction distance of sea urchins is 10âcm (images in figure by F. Di Trapani).
Figure 4. Conceptual model of the trophic cascades without the presence of MPAs, in their presence and in the Ustica case study.In areas where fishing is allowed, low densities of Diplodus causes the outbreak of sea urchin and consequently barren grounds are common. MPAs with their no-take policy are instead characterized by high densities of Diplodus that control urchins and allow algal canopy to return. The peculiar case of the Ustica MPA consists instead of low densities of Diplodus but, at the same time, extended algal coverage and low densities of sea urchins. In this case the seastar M. glacialis interacts with the ornate wrasse T. pavo and thus is able to heavily and successfully prey upon urchins species P. lividus and A. lixula and control their populations (images in figure by C. Bonaviri, F. Di Trapani and P. Gianguzza).
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