Coralline Barrens Research Articles

Coralline barrens and benthic mega-invertebrates: An intimate connection

Despite considerable progress in understanding the transition from algal forests to coralline barrens, knowledge of coralline barren ecosystems in terms of community composition and functioning is still sparse and important gaps remain to be filled. Using a barren/forest patch system, we tested the hypothesis that the presence of coralline barren enhances the abundance and diversity of benthic mega-invertebrates. We also analysed trophic functional diversity through isotopic analyses of δ13C and δ15N. The distribution of benthic mega-invertebrates biomass differed markedly between coralline barren and algal forest, being more abundant and diverse in the barren state. Isotopic diversity metrics of the benthic mega-invertebrates assemblage indicated comparable trophic structure between the two states, although higher isotopic uniqueness in coralline barren was determined by sea urchins, especially A. lixula, and carnivorous starfish. We showed that in a patchy coralline barren/algal forest system, a more diversified benthic mega-invertebrates assemblage in the barren caused limited trophodynamic changes. This was possibly determined by the behaviour of some trophic groups such as filter feeders, deposit feeders and omnivores. Finally, our results evidence the close association between coralline barrens and benthic mega-invertebrates, contradicting the common view of coralline barrens as depauperate habitats with low diversity and productivity.

Nutrient enrichment stimulates herbivory and alters epibiont assemblages at the edge but not inside subtidal macroalgal forests

Nutrient enrichment is a major threat to subtidal macroalgal forests. Several studies have shown that nutrient inputs can enhance the ability of opportunistic algal species to acquire space freed by disturbance, at the expense of architecturally complex species that form forests. However, competition between canopy- and turf-forming macroalgae is not limited to the aftermath of disturbance. Canopy-forming macroalgae can provide suitable substratum for diverse epibiont assemblages, including both algae (epiphytes) and sessile invertebrates (epizoans). Despite evidence of enhanced epiphyte loading under eutrophic conditions, few experimental studies have assessed how nutrient enrichment influences the structure of epibiont assemblages on canopy-forming macroalgae at the edge versus inside forests. In oligotrophic waters of the NW Mediterranean, we experimentally tested the hypothesis that nutrient-driven proliferation of opportunistic epiphytic algae would affect the performance of the fucoid, Carpodesmia brachycarpa, and reduce the richness and abundance of the epizoan species they support. We predicted negative effects of nutrient enrichment to be greater at the edge than inside forests and on thalli that had recovered in cleared areas than on those within undisturbed canopy stands. Nutrient enrichment did not affect the photosynthetic efficiency and reproductive output of C. brachycarpa. By contrast, it enhanced herbivore consumption and decreased the cover and diversity of epizoans at forest edges, likely by stimulating the foraging activity of Arbacia lixula, the most abundant sea urchin in adjacent encrusting coralline barrens. Fertilization of areas inside forests had no effect on either C. brachycarpa or epibiont assemblages. Finally, nutrient enrichment effects did not vary between cleared and undisturbed areas. Our results show that moderate nutrient enrichment of oligotrophic waters does not necessarily cause the proliferation of epiphytes and, hence, a strengthening of their competitive effects on canopy-forming macroalgae. Nevertheless, enhanced herbivory damage to fertilized thalli at forest edges suggests that fragmentation could reduce the resilience of macroalgal forests and associated epibiont assemblages to nutrient enrichment.

The role of wave-exposure and human impacts in regulating the distribution of alternative habitats on NW Mediterranean rocky reefs

The global decline of canopy-forming macroalgae has stimulated research on the mechanism regulating shifts among alternative habitats on rocky reefs. The effects of sea urchin grazing and alterations of environmental conditions are now acknowledged as the main drivers of shifts between canopy-formers and encrusting coralline barrens and algal turfs, respectively. The conditions under which these mechanisms operate remains, however, somewhat elusive. This is mostly a consequence of the fact that our current understanding has been generated by envisioning habitat shifts as dichotomic, at odds with rocky reef landscapes being composed by mosaics of habitats and with evidence of strong interactions among the species that compose each of the alternative habitats. Using data from a long-term sampling program and path analysis, we investigated how wave-exposure and human-induced degradation of environmental conditions regulate the mechanisms maintaining algal canopies formed by Cystoseira crinita, barren habitats and algal turfs as alternative states on subtidal reefs in the NW Mediterranean. In the Tuscan Archipelago, wave-exposure had positive effects on sea urchins, which, likely due to their low mean density, had weak effects on each of the alternative habitats. Canopy-forming macroalgae resulted, instead, to exert strong negative effects on the abundance of algal turfs. Since data from the Tuscan Archipelago did not explain any of the variation in the abundance of C. crinita canopies, a further analysis was performed including data from the coast of Tuscany to assess the role of cumulative human impacts in regulating habitat shifts. This showed that degradation of environmental conditions is a direct cause of the decline of macroalgal canopies, indirectly favouring the dominance of algal turfs. Our study suggests that management of human impacts should be considered a priority for preserving subtidal canopies formed by Cystoseira in the NW Mediterranean and that conservation efforts based exclusively on the control of sea urchin populations might be doomed to failure in some areas.

Pulses of phytoplanktonic productivity may enhance sea urchin abundance and induce state shifts in Mediterranean rocky reefs

This paper tests the hypothesis that increased planktonic primary productivity may enhance sea urchin recruitment and trigger changes in the structure of benthic communities in oligotrophic temperate regions. Underwater surveys were conducted in the marine reserve of northern Minorca (Balearic Archipelago, western Mediterranean) and an adjoining control area in 2005 and 2012 to assess the abundance of fishes and sea urchins and the cover of macroalgae before and after a natural pulse of planktonic primary productivity. The biomass of most fishes, including that of sea urchin predators, increased significantly in the whole area two years after the productivity pulse, without any effect of management or depth. The abundance of sea urchins also increased throughout the whole area two years after the productivity pulse, but the average test diameter decreased, thus revealing improved recruitment. The aggregated cover of erect algae and that of Cystoseira brachycarpa did not change significantly from 2005 to 2012, but the cover of turf-forming algae was negatively correlated with the biomass of sea urchins, whereas the cover of coralline barren was positively correlated with the biomass of sea urchins. The overall evidence indicates that planktonic primary productivity is a key factor in the dynamics of sea urchin populations in oligotrophic regions and that improved sea urchin recruitment after productivity pulses in spring and early summer may result in sea urchin populations sufficiently dense to result in the development of coralline barrens independently on the density of sea urchin predators.

Functional traits of two co-occurring sea urchins across a barren/forest patch system

Temperate rocky reefs may occur in two alternative states (coralline barrens and erect algal forests), whose formation and maintenance are often determined by sea urchin grazing. The two sea urchin species Paracentrotus lividus and Arbacia lixula are considered to play a similar ecological role despite their differing morphological traits and diets. The patchy mosaic areas of Ustica Island, Italy, offer an ideal environment in which to study differences in the performance of P. lividus and A. lixula in barren versus forest states. Results show that the two sea urchin species differ in diet, trophic position, grazing adaptation, movement ability and fitness in both barren and forest patches. We confirmed herbivory in P. lividus and omnivory with a strong tendency to carnivory in A. lixula. When the sea urchin escape response to a predator was triggered, P. lividus responded faster in barren and forest patches. Forest patch restricted movement, especially in A. lixula (velocity in barren ≈10-fold greater than in forest). A large Aristotle's lantern, indicative of durophagy, confirmed adaptation of A. lixula to barren state.

Italian marine reserve effectiveness: Does enforcement matter?

Marine protected areas (MPAs) have become popular tools worldwide for ecosystem conservation and fishery management. Fish assemblages can benefit from protection provided by MPAs, especially those that include fully no-take reserves. Fish response to protection can thus be used to evaluate the effectiveness of marine reserves. Most target fish are high-level predators and their overfishing may affect entire communities through trophic cascades. In the Mediterranean rocky sublittoral, marine reserves may allow fish predators of sea urchins to recover and thus whole communities to be restored from coralline barrens to macroalgae. Such direct and indirect reserve effects, however, are likely to be related to the enforcement implemented. In Italy, many MPAs that include no-take reserves have been declared, but little effort has been spent to enforce them. This is a worldwide phenomenon (although more common in some regions than others) that may cause MPAs and reserves to fail to meet their targets. We found that 3 of 15 Italian marine reserves investigated had adequate enforcement, and that patterns of recovery of target fish were related to enforcement. No responses were detected when all reserves were analyzed as a whole, suggesting enforcement as an important factor to be considered in future studies particularly to avoid that positive ecological responses in properly managed reserves can be masked by neutral/negative results in paper parks. Positive responses were observed for large piscivores (e.g. dusky groupers) and sea urchin predators at reserves where enforcement was effective. Those reserves with low or null enforcement did not differ from fished areas.

Potential of Marine Reserves to Cause Community‐Wide Changes beyond Their Boundaries

Fishing and other human activities can alter the abundances, size structure, and behavior of species playing key roles in shaping marine communities (e.g., keystone predators), which may in turn cause ecosystem shifts. Despite extensive evidence that cascading trophic interactions can underlie community-wide recovery inside no-take marine reserves by protecting high-level predators, the spatial extent of these effects into adjacent fished areas is unknown. I examined the potential for community-wide changes (i.e., the transition from overgrazed coralline barrens to macroalgal beds) in temperate rocky reefs within and around a no-take marine reserve. For this purpose I assessed distribution patterns of predatory fishes, sea urchins, and barrens across the reserve boundaries. Predatory fishes were significantly more abundant within the reserve than in adjacent locations, with moderate spillover across the reserve edges. In contrast, community-wide changes of benthic assemblages were apparent well beyond the reserve boundaries, which is consistent with temporary movements of predatory fishes (e.g., foraging migration) from the reserve to surrounding areas. My results suggest that no-take marine reserves can promote community-wide changes beyond their boundaries.

Marine Reserves Reestablish Lost Predatory Interactions And Cause Community Changes In Rocky Reefs

In the last decades, marine reserves have dramatically increased in number worldwide. Here I examined the potential of no-take marine reserves to reestablish lost predatory interactions and, in turn, cause community-wide changes in Mediterranean rocky reefs. Protected locations supported higher density and size of the most effective fish preying on sea urchins (the sea breams Diplodus sargus and D. vulgaris) than unprotected locations. Density of sea urchins (Paracentrotus lividus and Arbacia lixula) was lower at protected than at unprotected locations. Size structure of P. lividus was bimodal (a symptom of predation on medium-sized urchins) only at the protected locations. Coralline barrens were less extended at protected than at unprotected locations, whereas turf-forming and erect-branched algae showed an opposite pattern. Erect-unbranched and erect-calcified algae and conspicuous zoobenthic organisms did not show any pattern related to protection. Tethering experiments showed that predation impact on urchins was (1) higher at protected than at unprotected locations, (2) higher on P. lividus than on A. lixula, and (3) higher on medium-sized (2-3.5 cm test diameter) than large-sized (>3.5 cm) urchins. Sea urchins preyed on by fish in natural conditions were smaller at unprotected than at protected locations. The analysis of sea urchin remains found in Diplodus fish stomachs revealed that medium-sized P. lividus were the most frequently preyed upon urchins and that size range of consumed sea urchins expanded with increasing size of Diplodus fish. These results suggest that (1) depletion and size reduction of predatory fish caused by fishing alter patterns of predation on sea urchins, and that (2) fishing bans (e.g., within no-take marine reserves) may reestablish lost interactions among strongly interactive species in temperate rocky reefs with potential community-wide effects.

CASCADING HUMAN IMPACTS, MARINE PROTECTED AREAS, AND THE STRUCTURE OF MEDITERRANEAN REEF ASSEMBLAGES

Coastal marine assemblages are shaped by interactions between physical factors, biological interactions, and almost ubiquitously, human impacts. Large-scale manipulations of human access replicated over a range of physical and biological conditions can generate insights over the processes shaping marine assemblages. We examined the relative roles of human impacts and hydrographic conditions on assemblages of shallow (3–10 m depth) rocky reefs by comparing no-take reserves with fishing areas occurring in gradients of exposure of the coastline to dominant winds and waves around two Mediterranean islands, Capraia and Giannutri, Italy. We hypothesized that fishing influences assemblages directly by reducing populations of target fish species, and indirectly by reducing predation on sea urchins, intensifying herbivory, and causing “barrens” of encrusting coralline algae. We examined how the possible effects of fishing varied with physical exposure of the coastline. The composition of fish assemblages differed significantly between sites within no-take reserves and fished reference sites. Abundances and sizes of predatory fishes targeted by local fisheries were greater in no-take reserves than in fished areas. Sea urchin densities, the extent of coralline barrens, and the structure of the algal and invertebrate benthic assemblages showed clear variation associated with exposure of the coastline to dominant winds and waves, but weak effects of protection from human use. Densities of the black sea urchin Arbacia lixula were significantly greater along the windward than along the leeward sides of the islands, and were positively correlated with the extent of coralline barrens. In contrast, the purple sea urchin Paracentrotus lividus was more abundant along the leeward sides of islands and showed indirect responses to protection at Giannutri, where purple sea urchins tended to have greater densities at fished than at protected sites. Protection from fishing influenced fish assemblages directly, and benthic assemblages indirectly, but the latter effect was observed only at sites with lower physical exposure. Indirect effects of fishing and recovery of assemblages within marine protected areas through cascading trophic interactions are likely to vary depending on local physical conditions and on the characteristics of species that are locally dominant.

Temporal and spatial variability in settlement of the sea urchin Paracentrotus lividus in the NW Mediterranean

Settlement into the benthic habitat may be an important process in regulating sea urchin abundance, which potentially modifies the structure of benthic communities. Strong settlement events may increase sea urchin abundance beyond a certain threshold, leading to the formation of coralline barrens (overgrazed communities with a dominance of encrusting coralline algae). To understand the role of settlement in regulating sea urchin populations we first need to determine settlement variability. Temporal variation in settlement of the sea urchin Paracentrotus lividus was monitored at three sites in the Medes Islands, NW Mediterranean, during three settlement seasons (March 1998 through October 2000). Spatial variation in settlement was studied in 1999 at 50 sites along a gradient of exposures to waves and currents, inside and outside the archipelago, and separated by distances from tens to thousands of meters. Bathymetric distribution of settlement was also studied in 2000 at six sites at 5, 10, 15 and 20 m depths. Settlement of P. lividus occurred in a single annual peak within 3 weeks in May–June. Differences in settlement between years were more than two orders of magnitude. Spatial variability was found at all scales investigated, showing strong patchiness at the smallest spatial scales (tens of meters). Sea urchins settled preferentially at depths between 5 and 10 m. Substratum type, level of protection, and adult population densities were not significant in determining settlement. However, settlement was found to be related to the degree of exposure to waves and currents, indicating that physical processes are very important at the spatial scales investigated. This greatly variable settlement is a necessary, although not sufficient, condition to create gradients of adult P. lividus abundance. Further studies should be designed to investigate the interaction between settlement strength and post-settlement mortality.

Distribution patterns of sea urchins and barrens in shallow Mediterranean rocky reefs impacted by the illegal fishery of the rock-boring mollusc Lithophaga lithophaga

Shallow rocky habitats in SW Apulia (SE Italy, Mediterranean Sea) were surveyed in late spring 2002 to assess distribution patterns of sea urchins (Paracentrotus lividus and Arbacia lixula) and barren habitats (coralline barrens and bare substrates) in rocky reefs impacted by the destructive fishery of the rock-boring date-mussel Lithophaga lithophaga. Sea urchin density, test size-structure and biomass, and the percent cover of barrens were evaluated at four locations (5–6 km apart from each other), two heavily impacted by the date-mussel fishery and two controls. Sea urchin density and barren habitat cover were assessed at two and three sites (100–300 m apart), respectively, within each location. Sea urchin biomass was evaluated only at the scale of locations. Average density of P. lividus did not significantly change between impacted locations and controls, whereas A. lixula showed a greater density at the impacted locations. Distribution patterns of A. lixula, in addition, differed at the spatial scale of a few metres between impacted locations and controls, being generally more aggregated at the controls. The size-frequency distribution (test diameter) of P. lividus showed a mode at 3–4 cm at the impacted locations compared to a mode at 2–3 cm in the controls. The size-frequency of A. lixula was bimodal at the damaged locations (with modes at 1–2 and 4–5 cm, respectively) and unimodal (with the mode at 4–5 cm) at the controls. Average biomass of both sea urchins (P. lividus and A. lixula) was two- to fourfold greater at the impacted locations (~600 g wet wt m−2) than at the controls (150–250 g wet wt m−2). Barren habitats had a far greater average cover (mainly of macroalgae) at the impacted locations (from 79% to 96%) than at control locations (from 7% to 21%). These results show that the date-mussel fishery may have the potential to affect distribution patterns of sea urchins and to greatly enhance the percent cover of barren grounds in shallow Mediterranean rocky reefs.

Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management

An important principle of environmental science is that changes in single components of systems are likely to have consequences elsewhere in the same systems. In the sea, food web data are one of the few foundations for predicting such indirect effects, whether of fishery exploitation or following recovery in marine protected areas (MPAs). We review the available literature on one type of indirect interaction in benthic marine ecosystems, namely trophic cascades, which involve three or more trophic levels connected by predation. Because many indirect effects have been revealed through fishery exploitation, in some cases we include humans as trophic levels. Our purpose is to establish how widespread cascades might be, and infer how likely they are to affect the properties of communities following the implementation of MPAs or intensive resource exploitation. We review 39 documented cascades (eight of which include humans as a trophic level) from 21 locations around the world; all but two of the cascades are from shallow systems underlain by hard substrata (kelp forests, rocky subtidal, coral reefs and rocky intertidal). We argue that these systems are well represented because they are accessible and also amenable to the type of work that is necessary. Nineteen examples come from the central-eastern and north-eastern Pacific, while no well-substantiated benthic cascades have been reported from the NE, CE or SW Atlantic, the Southern Oceans, E Indian Ocean or NW Pacific. The absence of examples from those zones is probably due to lack of study. Sea urchins are very prominent in the subtidal examples, and gastropods, especially limpets, in the intertidal examples; we suggest that this may reflect their predation by fewer specialist predators than is the case with fishes, but also their conspicuousness to investigators. The variation in ecological resolution amongst studies, and in intensity of study amongst systems and regions, indicates that more cascades will likely be identified in due course. Broadening the concept of cascades to include pathogenic interactions would immediately increase the number of examples. The existing evidence is that cascade effects are to be expected when hard-substratum systems are subject to artisanal resource exploitation, but that the particular problems of macroalgal overgrowth on Caribbean reefs and the expansion of coralline barrens in the Mediterranean rocky-sublittoral will not be readily reversed in MPAs, probably because factors other than predation-based cascades have contributed to them in the first place. More cascade effects are likely to be found in the soft-substratum systems that are crucial to so many large-scale fisheries, when opportunities such as those of MPAs and fishing gradients become available for study of such systems, and the search is widened to less conspicuous focal organisms such as polychaetes and crustaceans.

Fishing, Trophic Cascades, and the Structure of Algal Assemblages: Evaluation of an Old but Untested Paradigm

Removal of important predators by fishing can result in trophic cascades and indirect effects on marine benthic communities. Indirect effects are especially evident when prey populations released from predation by fishing have the ability to modify entire benthic communities as do sea urchins Sea urchins have been shown to dramatically alter the underwater landscape by grazing, by converting stands of large erect algae into coralline barrens. In the western Mediterranean, a recent extension of coralline barrens into areas formerly dominated by erect algal assemblages has been attributed to release of predation on sea urchins by overfishing. Most suggestions concerning the transition form erect algeal assemblages to coralline barrens, however, have been speculative, and little descriptive and experimental work has been carried out to verify the hypothesis that fish predation on sea urchins (and its subsequent release by overfishing) drives this transition. Here we critically review the literature concerning the effect of fishing on sea urchin populations and its subsequent maintenance of different algal assemblages in the Mediterranean. The extant data cannot refute the fishes as important predators model. but we argue that other processes trecruitment, pollution, disease, large-scale oceanographic events, sea urchin harvesting, food subsidies, and availability of shelters) may also be important in regulating the structure of Mediterranean algal assemblages.

Inference in Ecology: The Sea Urchin Phenomenon in the Northwestern Atlantic

We have reviewed the considerable body of research into the sea urchin phenomenon responsible for the alternation between macroalgal beds and coralline barrens in the northwestern Atlantic. In doing so, we have identified problems with both the scientific approach and the interpretation of results. Over a period of approximately 20 years, explanations for the phenomenon invoked four separate scenarios, which changed mainly as a consequence of extraneous events rather than experimental testing. Our specific concerns are that results contrary to the keystone-predator paradigm for the American lobster were circumvented, system components of the various scenarios became accepted without testing, and modifications of some components appeared arbitrary. Our review illustrates dilemmas that, we suggest, have hindered ecological progress in general. We argue for a more rigorous experimental approach, based on sound natural-history observations and strong inference. Moreover, we believe that the scientific communi...

Experimental evaluation of aggregation behavior in the sea urchin Strongylocentrotus droebachiensis

Defensive aggregation by Strongylocentrotus droebachiensis has been invoked as the fulcrum for the transformation of macroalgal beds into coralline barrens in the northwest Atlantic. We critically examined some of the mechanisms contributing to aggregation behavior by experimentally manipulating sea urchins, purported predators and food during autumn 1983 and spring 1984 both in the laboratory and field. We utilized several approaches to examine a range of sea urchin responses to the presence of food, tethered predators, caged predators, crushed con-specifics in the field and predators in laboratory tanks. Some of the field cages had the property of allowing free passage to sea urchins while retaining lobsters; this allowed distinctions to be made between artifacts caused by cage walls or topographic barriers and unrestricted behavioral responses of sea urchins. The results falsified the hypothesis that aggregations of S. droebachiensis are elicited by predators. Except in the presence of algae, sea urchins always avoided decapod predators (but not sea stars) and fled from the vicinity of injured conspecifics. However, avoidance behavior was subordinate to feeding responses, demonstrated by mass migrations of sea urchins into cages (with lobsters) to feed on algae. We reaffirmed by observation and manipulation previous studies which showed that sea urchins aggregate only in the presence of food. Two types of sea urchin groupings were delineated: (1) surficial two dimensional associations, often caused by topographic or other features which inhibited dispersal and (2) cohesive three-dimensional aggregations induced by food.