Evaluating the effects of protection on fish predators and sea urchins in shallow artificial rocky habitats: a case study in the northern Adriatic Sea

Man-made defence structures (e.g., breakwaters, jetties) are becoming common features of marine coastal landscapes all around the world. The ecology of assemblages of species associated with such artificial structures is, however, poorly known. In this study, we evaluated the density and size of fish predators of echinoids (i.e., Diplodus sargus, Diplodus vulgaris, Sparus aurata), and the density of sea urchins (i.e., Paracentrotus lividus) at defence structures (i.e., breakwaters) inside and outside the marine protected area of Miramare (northern Adriatic Sea) in order to: (1) assess possible differences in fish predator density and size between protected and fished breakwaters; (2) assess whether fish predation may have the potential to affect sea urchin density in artificial rocky habitats. Surveys were carried out at four random times over a period of two years. Total density, and density of medium- and large-sized individuals of the three predatory fishes were generally greater at the protected than at the fished breakwaters, whereas no differences were detected in the density of small-sized individuals. Density of the sea urchin P. lividus did not show any difference between protected and fished breakwaters. The results of this study suggest that: (1) protection may significantly affect predatory fishes in artificial rocky habitats; (2) differences in predatory fish density, and size may be unrelated with the density of the sea urchin P. lividus; (3) protected artificial structures such as breakwaters, originally planned for other purposes, could represent a potential tool for fish population recovery and enhancement of local fisheries.     

The operational sex ratio of the sea urchin Paracentrotus lividus populations: the case of the Mediterranean marine protected area of Ustica Island (Tyrrhenian Sea, Italy)

We investigated, with a series of field and laboratory observations, the possible effect of the starfish Marthasteria glacialis predation on the operational sex ratio (OSR), i.e. the number of sexually mature males divided by the total number of sexually mature adults of both sexes at any one time, of the edible sea urchin Paracentrotus lividus . The OSR was estimated three times during the sea urchin summer spawning period (July 2004, June 2005 and July 2006) on barren substrates of Ustica Island Marine Protected Area (Southern Tyrrhenian Sea, Italy). Four sites were selected: two characterized by high M. glacialis density (take zone C) and two controls with low starfish density (no-take zone A). Mature sea urchins were independently collected by SCUBA diving and sexed. The adult sex ratio was skewed towards males at high M. glacialis density sites, whereas it was balanced (1:1) at predator low-density sites. Results of sex-selective feeding experiments in the laboratory showed that females of P. lividus were more vulnerable to M. glacialis predation. These outcomes underline the possible importance of M. glacialis in regulating the OSR of P. lividus populations.     

Patterns of Activity of the Sea Urchin Paracentrotus lividus in the Bay of Port-Cros (Var, France, Mediterranean)

Abstract. Tagged individuals of the sea urchin Paracentrotus lividus followed in Port Cros Island showed mostly nocturnal movements, with individual peaks of activity which were not coordinated for the population during the night period. The straight line distance travelled in 24 h has a mean value of 49 cm, with a range of 0 to 240 cm. Neither sea urchin size nor depth affect activity. The urchins living on rocky substrate moved significantly more than those on seagrass beds. From one day to another, the distance travelled by the population of urchins varies significantly; this is not related to season. The activity is negatively correlated with the mean wind speed; during a period of turbulence lasting several hours, movement was significantly oriented to the deep. Periods of inactivity of 1 or 2 days were observed; they are not coordinated for the individuals followed, and the relation between feeding and movement is not clear. Urchins seem to stay in a quite small area, at least for some months.     

Resource Use by a Mediterranean Rocky Slope Fish Assemblage

Abstract. Resource partitioning has been intensely studied in fish assemblages of tropical reefs, whereas surprisingly little research has been conducted on the benthic Mediterranean. Here we describe the composition of a fish assemblage of the rocky slopes at Tremiti Islands, southern Adriatic Sea, the vertical distribution at depths from 0 to 42 m, habitat choice and food use of the different species, and we identify the resources along which species are ecologically segregated. Species composition and fish density showed high similarities with the few other assemblages that have been censused on the rocky coasts of the Mediterranean. We observed a wide overdispersion among species in their use of food and habitat, while very little segregation occurred at the level of depth distribution. No coincident use of food, habitat or active periods occurred among fish species, and no trophic guilds exist in the three-dimensional niche.     

The other 93%: trophic cascades,stressors and managing coastlines in non-marine protected areas

Abstract

This paper reviews interactions involving stands of macroalgae on rocky reefs, and presents new data on changing sea surface temperatures (SSTs), as a contribution to the celebration of the fiftieth anniversary of the Leigh Marine Laboratory (LML) of the University of Auckland. The focus is on trophic interactions involving predators, sea urchins and large brown algae, particularly trophic cascades. Of the 369 publications arising from work at LML, 40 have been on key aspects of these trophic interactions. Quantitative investigations of the structure of kelp bed communities and mechanistic studies involving manipulative field-based experiments, essentially a bottom-up perspective based on habitats and key species, dominated the research through the 1980s. From the mid-1990s onwards, the focus was more on marine reserves and a hierarchical, top-down perspective of community structure, with a particular focus on the role of predatory fish, and marine reserves as a tool of management. I discuss these models of community structure of kelp beds within the wider context of the New Zealand nearshore zone, the varying biogeographic regimes around the coastline, diffuse stressors and the changing nearshore climate. I show there appears to have been a significant warming trend in SST in northeast and northwest New Zealand over the past 30 years. I conclude that a trophic effects model is unlikely to apply to much of the coastline of New Zealand, and that a model involving multiple effects, including bottom-up forces, environmental and climatic influences, species' demographics, and catchment-derived sedimentation is more appropriate for kelp communities over most of the country. New management models are needed to safeguard marine resources and the services they provide.     

Low densities of sea urchins influence the structure of algal assemblages in the western Mediterranean

Numerous studies of interactions between urchins and algae in temperate areas have shown an important structuring effect of sea urchin populations. These studies focused almost wholly on the effect of high urchin densities on laminarian forests. In contrast, algal communities below 5–6 m depth in the northwestern Mediterranean are characterised by low sea urchin densities (<5 ind m⁻²) and the absence of laminarian forests. No previous research has addressed sea urchin/algal interactions in this type of community. To determine the effect of the most abundant echinoid species, Paracentrotus lividus, on well-established algal communities in this area, we performed a removal–reintroduction experiment in rocky patches located between 13 and 16 m depth in the northwestern Mediterranean, where sea urchin densities ranged between 0.9 and 3.4 ind m⁻². After 6 months, the cover of non-crustose algae was significantly higher in the plots from which sea urchins had been removed than in control plots (84 vs 67% cover). These removal plots reverted to their original state upon reintroduction of sea urchins. The non-crustose algae consisted of turfing and frondose forms, with the former representing some 70% of the non-crustose algal cover. Change in the cover of turfing algae was responsible for the significant increase in algal development in the sea urchin removal plots. The response of frondose algae to the treatment varied between algal species. It is concluded that grazing by P. lividus exerts a significant effect on habitat structure, even in communities with low sea urchin densities, such as those found in vast areas of the Mediterranean sublittoral.     

Effects of sea urchin (Evechinus chloroticus) grazing in Dusky Sound,Fiordland, New Zealand

Evechinus chloroticus (Val.) is known to be an important grazer of subtidal barren habitats in northern New Zealand but its role in structuring rocky reef communities at colder southern localities is poorly understood. The present study was prompted by a proposal for the establishment of an E. chloroticus fishery in Dusky Sound, Fiordland, New Zealand. To determine the ecological importance of E. chloroticus in Dusky Sound, sea urchins were experimentally removed from shallow fucoid fringe (upper zone), mid‐depth barrens (middle zone), and deeper algal meadow (lower zone), at eight sites and compared with a paired set of eight control sites. Two years of continuous removal of E. chloroticus resulted in conspicuous changes to the algal community at all depth zones examined. The density of fucoid algae (Carpophyllum spp., Sargassum spp., Cystophora spp., and Landsburgia quercifolia) increased mostly in the upper and middle zones, although smaller increases were also observed in the lower zone. Changes in cover of herbaceous, turfing and crustose algae observed in the middle and lower zones were larger than in the upper zone. Density increases of the kelp Ecklonia radiata were observed mainly in the lower zone, although still important in the middle zone. These results show that E. chloroticus can have a strong influence on the structure of algal assemblages in Dusky Sound hence the development of an E. chloroticus fishery in this area should be treated with caution.     

Impacts of temperature anomalies on mortality of benthic organisms in the Adriatic Sea

Recurrent climate‐induced mass mortality episodes have been recorded in the Mediterranean Sea over the past 15 years, affecting rocky benthic communities. In this study, we provide for the first time a report on the annual mortality events of benthic sessile invertebrates occurring in the eastern part of the Adriatic Sea. Over the course of 14 consecutive years, we studied the sea temperature gradient to a depth of 40 m and found an abnormal summer warming trend and an increased frequency of above‐average temperatures. Mortality events were recorded in the summers of 10 observed years, in particular in 2009, when the highest mortality rates were recorded. Late in summer 2009, extensive mass mortality of sessile invertebrates was observed in the entire Eastern Adriatic Sea. We performed an analysis of selected target benthic species associated with mass mortality events with inter‐regional differences in hydrological and temperature conditions. We were able to characterize the mortality event by studying five areas covering the northern, central and southern regions of the Eastern Adriatic Sea. The degree of impact on each study area was quantified at 28 sites by estimating the proportion of affected target species. According to the obtained data, the northern sites (Cres area) were the least affected, whereas sites in the Central and Southern Adriatic [Tela??ica and Lastovo Nature Parks, Mljet National Park (NP)] displayed the highest impact. In summer 2009, sea surface temperatures reached values of 28 °C in the Cres area and 30 °C in Mljet NP. These thermal conditions were concomitant with moderate to severe mass mortalities of benthic populations. Mass mortality events reached depths of 45 m in most parts of the affected areas. Amongst studied species, the scleractinian coral and gorgonian populations suffered the most extensive damage during the mass mortality events.     

Habitat modification in tidepools by bioeroding sea urchins and implications for fine‐scale community structure

By creating novel habitats, habitat‐modifying species can alter patterns of diversity and abundance in marine communities. Many sea urchins are important habitat modifiers in tropical and temperate systems. By eroding rocky substrata, urchins can create a mosaic of urchin‐sized cavities or pits separated by exposed, often flat surfaces. These microhabitats appear to harbor distinct assemblages of species. We investigated how a temperate rocky intertidal community uses three small‐scale (<100 cm²) microhabitats created by or adjacent to populations of the purple sea urchin (Strongylocentrotus purpuratus): pits occupied by urchins, unoccupied pits, and adjacent flat spaces. In tidepools, flat spaces harbored the highest percent cover of algae and sessile fauna, followed by empty pits and then occupied pits. The Shannon diversity and richness of these sessile taxa were significantly higher in flat spaces and empty pits than in occupied pits. The composition of these primary space holders in the microhabitats also varied. Unlike primary space holders, mobile fauna exhibited higher diversity and richness in empty pits than in flat spaces and occupied pits, although results were not significant. The protective empty pit microhabitat harbored the highest densities of most trophic functional groups. Herbivores, however, were densest in flat spaces, concordant with high algal coverage. These results suggest the habitats created by S. purpuratus in addition to its biological activities alter community structure at spatial scales finer than those typically considered for sea urchins.     

Abundance and distribution of pelagic piscivorous fishes in the Columbia River plume during spring/early summer 1998-2003: Relationship to oceanographic conditions, forage fishes, and juvenile salmonids

From 1998 to 2003, we observed large fluctuations in the abundance and distribution of four pelagic predatory (piscivorous) fishes off northern Oregon and southern Washington, USA. Fluctuations in predatory fish species composition and abundance were strongly linked to the date of the spring transition and to ocean temperatures. Predatory fishes, forage fishes, and juvenile salmonids had distinct spatial distributions, with predators distributed primarily offshore and forage fish and salmonids onshore, but this varied depending on ocean conditions. We suggest that predatory and forage fish distributions respond to ocean temperatures, predator/prey interactions, and possibly turbidity. A shift in ocean conditions in 1999 decreased overall predator fish abundance in the Columbia River plume, particularly for Pacific hake. Marine survival of juvenile salmon started to increase in 1999, and forage fish densities increased in 2000, lagging by one year.     

The effects of trophic interactions and spatial competition on algal community composition on Hawaiian coral reefs

Much of coral reef ecology has focused on how human impacts change coral reefs to macroalgal reefs. However, macroalgae may not always be a good indicator of reef decline, especially on reefs with significant sea urchin populations, as found in Kenya and Hawaii. This study tests the effects of trophic interactions (i.e. herbivory by fishes and sea urchins) and spatial competition (between algae and coral) on algal community structure of reefs surrounding two Hawaiian Islands that vary in their level of human impacts. Reef‐building organisms (corals and crustose coralline algae) were less abundant and turf algae were more abundant on Maui as compared to Lanai, where human impacts are lower. In contrast to previous studies, we found no evidence that macroalgae increased with human impacts. Instead, low turf and macroalgal abundance were best explained by the interactive effects of coral cover and sea urchin abundance. Fishing sea urchin predators appeared to have cascading effects on the benthic community. The absence of sea urchin predators and high sea urchin densities correspond to a disproportionately high abundance of turf and crustose coralline algae. We propose that high turf algal abundance is a better indicator of reef decline in Hawaii than high macroalgal abundance because turf abundance was highest on reefs with low coral cover and few fish. The results of this study emphasize that understanding changes in community composition are context‐dependent and that not all degraded reefs look the same.     

Deep‐Sea Diversity: Overlooked Messages from Shallow‐Water Sediments

Abstract. Much of the discussion of high deep‐sea diversity has assumed that asymmetric inter‐specific competition will rapidly lead to the elimination of many species unless restrained by extensive differentiation of niches, or the action of predation and/or environmental disturbance. This is true for some habitats, including rocky shores. However, experimental studies indicate that marine soft sediment communities do not function like this. In shallow‐water sediments, competition is usually symmetric and relatively weak. Asymmetric competition that leads to the elimination of one species by another on time scales shorter than one generation is rare, apart from interactions that involve large‐scale modification or disturbance of the sediment. Competition is therefore relatively unimportant as a process structuring communities and the impact of predation is usually to reduce rather than enhance diversity. These results have been largely ignored by the literature on deep‐sea diversity. If deep‐sea communities function in similar ways, coexistence of many species within small areas on short time scales does not need further explanation. We do , however, need to explain why abundances of all species remain bounded on large spatial scales and time scales of several generations. The model of diversity maintenance proposed by Huston (1979) and applied to the deep sea by Rex (1983) achieves this by implicit intra‐specific, density‐dependent processes that increase the population growth rate of species that have become locally rare. This would give robust maintenance of diversity, but there is no evidence for density dependence of this type in the deep sea, and no plausible mechanisms by which it could occur. Alternative models require either spatial heterogeneity on a scale much larger than that envisaged by the grain‐matching hypothesis or the placing of a cap on the abundance of common species, perhaps by frequency‐dependent predation. Arbitrating between these possibilities will require assessments of the population dynamics and spatial distribution of individual species on spatial and temporal scales much greater than those usually considered in the deep sea.     

Movement patterns of the sea urchin Paracentrotus lividus in a marine reserve and an unprotected area in the NW Mediterranean

Sea urchins can alter the composition and dynamics of algal communities by grazing. Changes in their displacement capability can influence their grazing and thus their effect on algal communities. The daily and monthly movement of Paracentrotus lividus inside and outside a marine reserve in the NW Mediterranean Sea was studied in order to determine the role of predation in sea urchin movements and its potential grazing impacts. During the 3‐month study, the total distance travelled by sea urchins ranged from 71.8 to 673.6 cm (mean = 379.2 cm, SD = 221.3). Home ranges (distances from the initial position) were between 50 and 302 cm (mean = 150.7 cm, SD = 99.4). Movements were not directional but random, with a mean of 150 cm around the initial position. The activity of Paracentrotus lividus was significantly higher at night than during daylight. Total displacement at the end of the experiment was significantly higher in the unprotected area than in the reserve, as was the home range. The linear distance travelled in a 24‐h period ranged between 6 and 220 cm with a mean home range of 51 cm. These results agree with those of other authors, and allow us to rule out major migratory processes of sea urchin populations in this area. Nevertheless, these results underline the role of predatory fishes in reducing herbivory pressure by trophic cascades, reinforcing the evidence that sea urchin escape behaviour may be an important factor in structuring algal communities.     

An Analysis of the Coastal Fish Assemblage of the Ustica Island Marine Reserve (Mediterranean Sea)

A study of the coastal fish assemblages in the marine park of Ustica Island (Southern Tyrrhenian Sea, Mediterranean) was conducted from June 1994 to September 1995 and from June 1996 to September 1997. The principal aims of the research were to: (1) define the faunistic features of local fish communities; (2) assess the effectiveness of the protection regime of the marine park on the fish assemblages ('reserve effect'); (3) provide information on the distribution of some Epinephelus and Diplodus species in the shallowest depth zone of the island. During seasonal surveys, underwater visual censuses were carried out at several sites located in three zones of the island, each with a different level of protection. Observations were made along 250 m² transects at 3–5, 10–15 and 25–30 m depth ranges. Additional surveys were made by SCUBA diving and snorkelling. A statistically significant effect of depth on the fish community parameters was observed, whereas differences linked to protection level, zones, sites and seasons were not significant. The abundance and frequency of occurrence of some species, particularly dusky grouper Epinephelus marginatus , were positively correlated with the degree of protection of the different zones of the marine park. Certain sites of the island are important as nursery areas for three species of the genus Diplodus ( i.e., D. puntazzo, D. sargus and D. vulgaris ).     

The key role of the sea urchin Diadema aff. antillarum in controlling macroalgae assemblages throughout the Canary Islands (eastern subtropical Atlantic): an spatio-temporal approach

Diadema aff. antillarum performs a key role in organizing and structuring rocky macroalgae assemblages in the Canary Islands. Densities of D. aff. antillarum higher than 2 individuals m(-2) are found to drastically reduce non-crustose macroalgal cover to below 30% and wave exposure appears as a major factor determining sea urchin density, which decreases with exposure level. Substrates containing >20% sand limit urchin to under 1 individual m(-2) but high relief rocky habitats show higher density. Moreover, several anthropogenic factors (number of islanders and tourists per coastal perimeter, and number of operational fishing boats) were positively correlated with urchin abundance. A trend of increasing urchin density through time was found, although well structured marine systems found at Mar de Las Calmas Marine Protected Area and at the no-take area of La Graciosa Marine Protected Area do not seem to follow this general trend.     

Tidal variation in a rocky inter‐tidal fish population: the case of white seabream Diplodus sargus juveniles

The rocky inter‐tidal habitat is a harsh and fluctuating environment, subject to frequent disturbances. Field observations of juvenile white seabream Diplodus sargus in inter‐tidal rocky habitats were conducted to analyse the spatial distribution and feeding activity of this species in relation to the tidal cycle. The depth at which fish were observed did not change in most tidal phases while feeding activity changed with tidal level, showing the occurrence of tidal migrations and that feeding may be limited by habitat availability in shallow waters and thus be dependent on tidal changes. The present results show the exploitation of available feeding areas in the rocky inter‐tidal by juvenile white seabream, which corroborates the importance of these habitats for the first developmental stages of this fish species.     

Spatial variation patterns of subtidal seaweed assemblages along a subtropical oceanic archipelago: Thermal gradient vs herbivore pressure

The structure and composition of subtidal rocky seaweed assemblages were studied at 69 sites on the Canary Islands (northeastern Atlantic). This group of islands are situated at the southern boundary of the warm temperate region and adjacent to the cold waters from the northwest African coastal upwelling, which creates a difference of almost 2 °C in surface seawater temperature from the eastern to the western islands. This thermal variation allows an examination of the transition between the warm temperate and the tropical regions along this longitudinal gradient together with the hypothesised Fucales-dominated assemblages towards the eastern islands in contrast to the Dictyotales-dominated assemblages towards the western ones. Environmental and biological parameters were considered in order to investigate which were the main factors explaining spatial variation along the gradient in a multi-scaled approach. Although seventy-nine macroalgae were identified, 87.63% of the total mean cover was due to six taxa (Lobophora variegata, nongeniculate corallines, Canistrocarpus cervicornis, Jania adhaerens, Cystoseira abies-marina and Pseudolithoderma adriaticum). At a large scale, sea urchin density explained the highest variation in seaweed assemblages (26.94%), and its pattern of distribution across the islands. The expected pattern of distribution according to the upwelling distance only occurred in restricted areas of the Canarian Archipelago in absence of herbivore pressure and habitat degradation. Spatial variations within islands (medium scale) were mainly related to wave exposure, while at a small scale these were mostly due to the degree of sedimentation.     

Do Mediterranean fish assemblages associated with marine caves and rocky cliffs differ?

Fish assemblages associated with marine caves and rocky cliffs were investigated in the Salento Peninsula (SE Italy, Mediterranean Sea) by using visual census methods. Sampling was done at three sites, each of which included 4 habitat types: the external and the internal portions of caves, and shallow and deep rocky cliffs. 10 and 13 species were found exclusively inside cave habitats (e.g. Corcyrogobius lichtensteini, Thorogobius ephippiatus and Grammonus ater) or in rocky cliffs (e.g. Diplodus annularis, Sarpa salpa, Sparisoma cretense, Spondyliosoma cantharus), respectively. The four habitat types shared 10 species, and the external portions of the caves shared the most species (both with the internal cave portions and the external rocky cliffs). As a general rule, dissimilarity in the fish assemblage structure between habitats was far greater than dissimilarity between sites. Apogon imberbis (mostly associated with caves) and Chromis chromis (typifying rocky cliffs, mainly the deep ones) mostly contributed to dissimilarities between caves and rocky cliffs. Apogon imberbis (mostly associated with internal caves) and Coris julis (mainly associated to external cave portions) contributed strongly to dissimilarities between internal and external cave portions, while C. chromis, Symphodus mediterraneus and C. julis (associated with the deeper cliffs) and Thalassoma pavo (mostly present in shallow cliffs) differentiated deep and shallow cliffs. Diplodus vulgaris, Oblada melanura and Mullus surmuletus showed a marked increase in density during the cold season in the caves. These results show that fish assemblages associated with rocky reefs rich in marine caves (in terms of relative densities, species composition, species richness, exclusive species and presence of juveniles of some valuable species) may be affected by the peculiar ecological conditions within caves, which could provide additional resources for fishes (e.g. food availability, refuge against predators, sand patches within a rocky matrix) compared to rocky reefs without caves. These results suggest that stretches of rocky coasts rich in marine caves should be considered within management/conservation programs (e.g. when establishing Marine Protected Areas).     

Diversity and Distribution of the Bryozoa along Underwater Cliffs in the Adriatic Sea with Special Reference to Thermal Regime

Abstract.  The diversity and distribution of bryozoans have been surveyed at two localities, Cape Struga on Lastovo Island (South Adriatic) and Cape Šilo on Prvić Island near Senj (North Adriatic), with similar characteristics of topography and exposure but markedly different sea temperature conditions. Continuous measurements over one year have shown that temperature conditions differ in two aspects. First, the annual range of temperature is much larger in the North. Second, in the South during summer, marine life within the thermocline layer is exposed to large high-frequency temperature oscillations, partly due to an internal diurnal tide, a phenomenon recorded for the first time in the Adriatic. Altogether, 78 species have been recorded, 57 in Lastovo and 50 in Prvić, and 29 in both localities. The comparison of mean zooid lengths of 14 bryozoan species occurring at both localities indicates no consistent difference in zooid size between northern and southern sites. Seventeen bryozoan species have been recorded in the Eastern Adriatic Sea for the first time.     

Seasonal Variation in the Covering ­Behaviour of the Echinoid Paracentrotus lividus (Lamarck)

Abstract. Covering behaviour is displayed by several regular echinoid species but its functional significance has yet to be quantified. Some of the most popular theories have interpreted this behaviour as an adaptive response to avoid over-exposure to light and/or as an anti-predator strategy. Since both predation pressure and light intensity may be seasonal as well as diurnal in nature, the aim of the present study was to quantitatively examine, in situ , the potential seasonality of covering behaviour in the purple sea urchin, Paracentrotus lividus (Lamarck). Data were collected over a one-year period at Lough Hyne, Co. Cork in Ireland. A peak in covering activity was observed over the summer months. Predator density and light intensity (sunlight hours) were also shown to vary seasonally at Lough Hyne. Covering behaviour in P. lividus , as in other echinoids, may be a response to a number of simultaneously interacting factors. At Lough Hyne, however, light intensity and covering item availability appear to be particularly important factors.