Competition and habitat suitability: small-scale segregation underpins large-scale coexistence of key species on temperate rocky shores

Identifying the mechanisms that underpin species richness is one of the central issues of community ecology. On rocky shores in north-western Europe, two key limpet species coexist on the mid- and low shore but are segregated at small scales with respect to habitat. Short-term and long-term experiments were done to test whether habitat suitability or habitat-specific competition drives the small-scale segregation of these species and therefore underpins their coexistence at larger spatial scales. In a controlled short-term experiment, Patella vulgata was transplanted onto open rock and into pools that either contained Patella ulyssiponensis and/or their mucus or from which P. ulyssiponensis and/or their mucus had been removed. After 2 days, P. vulgata remained in all experimental plots in similar numbers irrespective of treatment indicating that there was no negative response to P. ulyssiponensis, mucus or the pool habitat. In a long-term experiment, cage enclosures containing both species were set up in pools and on open rock over a 6-month period. P. vulgata grew equally well on both open rock and in pools but suffered higher mortality in pools. P. ulyssiponensis showed lower growth rate and higher mortality on open rock than in pools. P. ulyssiponensis exhibited increased growth in higher intraspecific densities on open rock and reduced growth in higher intraspecific densities in pools, indicating some degree of intraspecific facilitation on open rock and intraspecific competition in pools. There was no evidence of interspecific competition either in the short term or in the long term. Results revealed that habitat suitability was the mechanism causing segregation of these species at smaller spatial scales enabling them to coexist at larger spatial scales. Conflicting results in the short-term and long-term experiments highlight the importance of considering the correct temporal extent for experimental tests of hypotheses.     

Food supply, grazing activity and growth rate in the limpet Patella vulgata L.: a comparison between exposed and sheltered shores

The limpet Patella vulgata L. is an important microphagous grazer on intertidal rocky shores of north-west Europe, occurring across the wave exposure gradient. Groups of P. vulgata were selected at mid-tide level of two exposed shores and two sheltered, fucoid dominated shores on the Isle of Man, British Isles, and manipulated to equivalent densities and population structure. The level of grazing activity and growth rate were determined over a 1-year period. At the same time, the abundance of epilithic microalgae, measured as the concentration of chlorophyll a, was determined as an estimate of food supply. Microagal abundance showed a seasonal pattern in both exposed and sheltered conditions, with higher levels in winter compared to summer. In both seasons, the microalgal resource was more abundant on the sheltered shore studied. The level of grazing activity in P. vulgata showed a seasonal pattern on the exposed but not the sheltered shores. Averaged over the year, grazing activity on the exposed shores was over double that on sheltered shores. Thus, in sheltered conditions, food supply for limpets was high and grazing activity low; in exposed conditions, food supply was low and grazing activity high. The growth rate of P. vulgata, measured as increase in shell length, showed no significant difference between exposed and sheltered shores. Growth rate was also determined in P. vulgata at natural densities. Although the overall density declined with decreasing exposure to wave action, the density per unit area of grazeable substance was higher in shelter. In these populations, the mean growth rate was over twice as high on exposed compared to sheltered shores.     

Consistent effects of consumer species loss across different habitats

Our knowledge of the effects of consumer species loss on ecosystem functioning is limited by a paucity of manipulative field studies, particularly those that incorporate inter‐trophic effects. Further, given the ongoing transformation of natural habitats by anthropogenic activities, studies should assess the relative importance of biodiversity for ecosystem processes across different environmental contexts by including multiple habitat types. We tested the context‐dependency of the effects of consumer species loss by conducting a 15‐month field experiment in two habitats (mussel beds and rock pools) on a temperate rocky shore, focussing on the responses of algal assemblages following the single and combined removals of key gastropod grazers (Patella vulgata, P. ulyssiponensis, Littorina littorea and Gibbula umbilicalis). In both habitats, the removal of limpets resulted in a larger increase in macroalgal richness than that of either L. littorea or G. umbilicalis. Further, by the end of the study, macroalgal cover and richness were greater following the removal of multiple grazer species compared to single species removals. Despite substantial differences in physical properties and the structure of benthic assemblages between mussel beds and rock pools, the effects of grazer loss on macroalgal cover, richness, evenness and assemblage structure were remarkably consistent across both habitats. There was, however, a transient habitat‐dependent effect of grazer removal on macroalgal assemblage structure that emerged after three months, which was replaced by non‐interactive effects of grazer removal and habitat after 15 months. This study shows that the effects of the loss of key consumers may transcend large abiotic and biotic differences between habitats in rocky intertidal systems. While it is clear that consumer diversity is a primary driver of ecosystem functioning, determining its relative importance across multiple contexts is necessary to understand the consequences of consumer species loss against a background of environmental change. Synthesis The roles of species may vary with environmental context, making it difficult to predict how biodiversity loss affects ecosystem functioning across multiple habitats. We tested how natural algal assemblages in two distinct intertidal habitats responded to the removal of different combinations of key consumer species. Despite an initial habitat‐dependent effect of consumer loss, habitat type did not modify the longer‐term responses of algal assemblages to either the identity or number of consumer species removed. Our findings show that, in certain systems, consumer diversity remains a primary driver of ecosystem functioning across widely different environmental contexts.     

Spatial and temporal variation of the fatty acid composition of Patella spp. (Gastropoda: Prosobranchia) soft bodies and gonads

This study evaluated the effects of season and spatial distribution on the fatty acid composition of Patella depressa gonads and Patella spp. soft body tissue. The results show that the quantitatively most important fatty acids were the saturated fatty acids (SFA) 16:0, 14:0 and 18:0; the monounsaturated fatty acids (MUFA) 18:1(n-7), 18:1(n-9), 16:1(n-7) and 20:1(n-9) and the polyunsaturated fatty acids (PUFA) eicosapentaenoic acid (EPA 20:5(n-3)), and arachidonic acid (ARA 20:4(n-6)). P. depressa and P. ulyssiponensis soft body fatty acid profiles revealed significant differences between sexes; males showed significantly higher percentages of PUFA, highly unsaturated fatty acids (HUFA), (n-3) fatty acids and ARA, while in females significantly higher proportions of MUFA were found. Analysis of variance on the fatty acid composition of P. depressa gonads revealed significant differences between sexes, which were more marked than when the whole body was analysed. Males showed a significantly higher percentage of PUFA, HUFA, fatty acids from the (n-3) and (n-6) series, ARA and EPA, while females were seen to have higher proportions of SFA, MUFA and total fatty acid methyl esters (FAME). Some variability was seen to occur due to shore location and seasons, but these effects were not so obvious.     

Large-scale coexistence and small-scale segregation of key species on rocky shores

Biodiversity is defined by the scales at which organisms coexist. Coexistence at larger spatial scales may be underpinned by segregation at smaller spatial scales or temporal variability in behaviour and/or distribution. Limpets of the genus Patella are keystone grazers controlling the growth of macro-algae on many rocky shores. This study examined the distribution and abundance of P. vulgata and P. ulyssiponensis in relation to habitat and to each other at a range of spatial scales. Limpets were sampled on four shores on each of the east and west coasts of Ireland, in two different transects (10 m apart) at each of three shore heights in winter 2003 and summer 2004. P. vulgata and P. ulyssiponensis coexist around the coast of Ireland, but on shores where they co-occur, the pattern of coexistence begins to break down at the level of shore height: P. ulyssiponensis were more abundant on the low-shore than mid-shore, and P. vulgata were distributed evenly throughout the low and the mid-shore. At the level of habitat (pools vs. open rock), the two species exhibited a high degree of segregation: P. vulgata of all sizes were more common on open rock and P. ulyssiponensis of all sizes were more common in pools. The presence or absence of P. ulyssiponensis had no effect on the distribution of juvenile P. vulgata with respect to pools. Unexpectedly, however, a greater proportion of adult P. vulgata were found in pools at sites where P. ulyssiponensis were present in the pools than at sites where they were absent. The results of this study emphasize the need for multiple-scale analyses of the distribution and abundance of organisms to understand the organisation of natural assemblages. Handling editor: K. Martens     

Grazing dynamics in intertidal rockpools: Connectivity of microhabitats

Differences between rockpool and emergent rock communities are often attributed to their contrasting physical conditions. However, differences in grazing pressure between rockpools and open rock could also exert an important structuring role. Greater densities and/or the lack of tidal constraints on foraging may allow grazing intensity to be greater in rockpools. Here, wax discs were deployed to compare grazing intensity between rockpool and emergent rock habitats at each of three tidal heights on a moderately exposed shore in SW England. Grazing intensity was then examined in relation to herbivore density. Grazing intensity in pools was twice that on emergent rock, despite a lower density of herbivores in the rockpools. Of these herbivores, patellid limpets are the dominant grazers on rocky shores throughout the NE Atlantic and are recognised to have a major role in structuring intertidal communities. Thus, subsequent experiments focussed on the influence of limpets in determining the differences in consumer pressure between rockpools and emergent rock. Three alternative explanations were considered: (1) the effect of continuous immersion on grazing intensity in rockpools; (2) differences in limpet species abundance between the two habitats; (3) movement of limpets from emergent rock into pools to feed. The level of grazing pressure exerted by Patella ulyssiponensis (Gmelin), the predominant species living constantly immersed in rockpools, was similar to that of P. vulgata (Linnaeus) which is predominantly found on emergent rock. P. vulgata were observed moving from emergent rock into rockpools during high tide. Manipulative experiments confirmed that these foraging excursions resulted in a 2-fold increase in grazing intensity in the pools. Grazing activity of P. vulgata in rockpools was not consistent between sites and may be influenced by differences in wave exposure and/or the abundance of microbial resources. Elevated consumer pressure in rockpools may be an important factor influencing algal assemblages and probably explains the predominance of grazer resistant-species in these pools.     

Impacts of sewage outfalls on rocky shores: Incorporating scale,biotic assemblage structure and variability into monitoring tools

Coastal systems, such as rocky shores, are among the most heavily anthropogenically-impacted marine ecosystems and are also among the most productive in terms of ecosystem functioning. One of the greatest impacts on coastal ecosystems is nutrient enrichment from human activities such as agricultural run-off and discharge of sewage. The aim of this study was to identify and characterise potential effects of sewage discharges on the biotic diversity of rocky shores and to test current tools for assessing the ecological status of rocky shores in line with the EU Water Framework Directive (WFD). A sampling strategy was designed to test for effects of sewage outfalls on rocky shore assemblages on the east coast of Ireland and to identify the scale of the putative impact. In addition, a separate sampling programme based on the Reduced algal Species List (RSL), the current WFD monitoring tool for rocky shores in Ireland and the UK, was also completed by identifying algae and measuring percent cover in replicate samples on rocky shores during Summer. There was no detectable effect of sewage outfalls on benthic taxon diversity or assemblage structure. However, spatial variability of assemblages was greater at sites proximal or adjacent to sewage outfalls compared to shores without sewage outfalls present. Results based on the RSL, show that algal assemblages were not affected by the presence of sewage outfalls, except when classed into functional groups when variability was greater at the sites with sewage outfalls. A key finding of both surveys, was the prevalence of spatial and temporal variation of assemblages. It is recommended that future metrics of ecological status are based on quantified sampling designs, incorporate changes in variability of assemblages (indicative of community stability), consider shifts in assemblage structure and include both benthic fauna and flora to assess the status of rocky shores.     

Mechanical wear of the gastropod radula: a scanning electron microscope study

The wear sustained by the teeth of the highly mineralized radula of Patella vulgata and the unmineralized radula of Agriolomax reticulatus has been studied with the scanning electron microscope. The unworn teeth of P. vulgata have tall pointed cusps and wear is first seen as a chipping of the tips then as abrasion. There is a well defined abraded surface giving the worn teeth a chisel shape. In cleaved teeth fibres ˜ 800 Å in diameter are observed parallel to the axis of the tooth. Evidence is presented for chemical etching and for the existence of a surface coat on the tooth. A. reticulatus teeth show wear over their whole surface. With the aid of the grooves in the jaw caused by the teeth the role of the jaw in flattening the radula and protracting and retracting the odontophore is confirmed. From the arrangement of the abraded surfaces on the teeth of P. vulgata it was deduced that the teeth rows are abraded one at a time while on a convex surface at or near the bending plane.     

Effects of grazer identity on the probability of escapes by a canopy-forming macroalga

Through their grazing activities limpets have an important role in controlling macroalgal abundance and as a result the structure and dynamics of rocky shore assemblages. Using two congeneric limpet species, with different biogeographic distributions, and whose ranges are expected to alter with climatic warming, we separated the magnitude of their grazing activity over time and the subsequent consequence for macroalgal growth.The northern/boreal limpet, Patella vulgata (L.), consistently grazed more than the southern/lusitanian limpet, P. depressa (Pennant), particularly during spring and summer when P. depressa was reproductively active. Individuals of Fucus vesiculosus (L.) that settled during this time were able to grow to a size where they escaped the grazing activities of P. depressa, resulting in mature F. vesiculosus being present in all P. depressa treatments. In contrast, P. vulgata, which was not reproductively active during this period, exhibited no reduction in its grazing activity and prevented macroalgae from growing in experimental treatments. It therefore appears that P. vulgata has a stronger role, than P. depressa, in controlling macroalgal abundance on shores of southwest Britain.We present a conceptual model highlighting the direct and indirect interactions between these two limpet species and F. vesiculosis. If as predicted, under current warming scenarios, P. depressa becomes the dominant limpet on shores of southwest Britain there will be subsequent changes in rocky shore community structure and ecosystem functioning. Our research emphasises that even closely related species with similar ecological niches can exhibit different behaviours that fundamentally alter their biological interactions with other organisms leading to idiosyncratic responses to predicted changes in climate.     

Equatorial range limits of an intertidal ectotherm are more linked to water than air temperature

As climate change is expected to impose increasing thermal stress on intertidal organisms, understanding the mechanisms by which body temperatures translate into major biogeographic patterns is of paramount importance. We exposed individuals of the limpet Patella vulgata Linnaeus, 1758, to realistic experimental treatments aimed at disentangling the contribution of water and air temperature for the buildup of thermal stress. Treatments were designed based on temperature data collected at the microhabitat level, from 15 shores along the Atlantic European coast spanning nearly 20° of latitude. Cardiac activity data indicated that thermal stress levels in P. vulgata are directly linked to elevated water temperature, while high air temperature is only stressful if water temperature is also high. In addition, the analysis of the link between population densities and thermal regimes at the studied locations suggests that the occurrence of elevated water temperature may represent a threshold P. vulgata is unable to tolerate. By combining projected temperatures with the temperature threshold identified, we show that climate change will likely result in the westward expansion of the historical distribution gap in the Bay of Biscay (southwest France), and northward contraction of the southern range limit in south Portugal. These findings suggest that even a minor relaxing of the upwelling off northwest Iberia could lead to a dramatic increase in thermal stress, with major consequences for the structure and functioning of the intertidal communities along Iberian rocky shores.     

Phylogeny and phylogeography of the genus Patella based on mitochondrial DNA sequence data

Although some molecular phylogenies of Patella species have been published in recent years, unresolved questions concerning the phylogeny and taxonomy of this genus still remain. We sequenced the mitochondrial genes cytochrome c oxidase subunit I, 12S rRNA and 16S rRNA for all Patella species (Patella vulgata, Patella depressa, Patella candei, Patella caerulea, Patella lugubris, Patella ferruginea, Patella pellucida and the continental and Macaronesian forms of Patella ulyssiponensis and Patella rustica) and Cymbula safiana. Our results revealed the occurrence of five strongly supported clades, although relationships between these are not well supported. According to our data P. vulgata is a genetically distinct lineage and the close phylogenetic relationship between this species and P. depressa, found in previous mitochondrial DNA studies, is not supported. The Mediterranean Sea and the Macaronesian Islands seem to have played an important role in the speciation and diversification of this genus, although different clades show different phylogeographic patterns. Our dataset point to the necessity of a taxonomic revision, as P. candei is paraphyletic relative to P. lugubris.     

Development of microsatellite loci for the black-footed limpet, <Emphasis Type="Italic">Patella depressa</Emphasis>, and cross-amplification in two other <Emphasis Type="Italic">Patella</Emphasis> species

Limpets (Patella spp.) are suitable organisms to investigate the effects of climate change in marine systems. They are widespread over NE Atlantic intertidal rocky shores and have been extensively studied in terms of population dynamics and ecology. Within genus Patella, microsatellites have only been developed for Patella caerulea and cross-species tests are unknown. In this work, we describe 11 primer pairs for Patella depressa and the results of cross-species testing on Patella candei and Patella rustica.     

The limpet Patella vulgata L. at night in air: effective feeding on Ascophyllum nodosum monocultures and stranded seaweeds

Opportunistically, the limpet Patella vulgata will switch frommicrophagous grazing to feeding on attached macroalgae or, anovel finding, on accumulations of stranded seaweeds. Macroalgalfood is ingested primarily at night during emersion, when thethalli come to lie on the rock surface and are sufficientlydamp. Monocultures of Ascophyllum nodosum are not immune tothe destructive effects of limpets as previously thought. Patellavulgata can graze them down to complete disappearance, thuspushing Ascophyllum back to refuges where P. vulgata is absentor rare. Such refuges were found along a wide range from verysheltered to strongly wave-exposed rocky shores in Brittany,France. By a combination of its macrophagous and microphagousfeeding habits, P. vulgata can control mid-tidal macroalgalassemblages in a similar fashion to the action of sea urchinsupon kelp communities inhabiting the lower intertidal and shallowsublittoral zones of rocky shores. (Received 30 October 2006; accepted 25 May 2007)     

Cell communication compartments in molluscan embryos

Early embryos of Patella vulgata have been injected with Lucifer Yellow. No restriction of dye spread was found. We show that later in the development, the larval trochophore stage present evidence of compartments of cell communication. These dye compartments coincide with different presumptive regions.     

The role of cyclins in the maturation of Patella vulgata oocytes.

We have cloned and sequenced the cDNAs encoding Patella vulgata cyclins A and B. The cDNA clones contain an open reading frame of 426 and 408 amino acids respectively, which present similarity with cyclins from other species. Cyclin A and B RNAs are present as polyadenylated and non-polyadenylated RNA in prophase oocytes and are completely polyadenylated in metaphase I. During the first cleavages after fertilization the level of cyclin A and B mRNAs is high and drops when the free swimming stage is reached. Using p13suc1-Sepharose bead precipitation we demonstrate that cyclin synthesis is triggered during maturation and that inhibition of protein synthesis makes the cyclins disappear rapidly from the metaphase I oocytes, which shift to interphase condition. By microinjecting antisense oligonucleotides into metaphase I oocytes, we demonstrate that in vivo ablation of cyclin A and B messengers together gives the same result, whereas microinjection of only one oligonucleotide does not show any effect.     

Genecological notes on Allium schoenoprasum L.

Summary

Ajuga pyramidalis is a polycarpic, perennial herb which is variable in flowering and population size. It has been recorded from over 200 sites in the Highlands and Islands of Scotland, one in the Lake District and in twelve coastal sites in Ireland. It grows mainly on circum-neutral soils (pH 4.9–6.9) in open grassland and heathland, and upland rock ledges. It does not appear to be under any particular threat in Britain.     

Sex change in the Mollusca

Sex change in the Mollusca is almost exclusively protandric (male to female), and has only been reported among gastropods and bivalves. The adaptive value of protandry in these two classes most likely relates to the limited availability of females, and the consequent size-independent nature of male reproductive success (versus the size-dependent nature of reproductive success in females). In two well studied distantly related prosobranch gastropod superfamilies, Calyptracea and Patellacea, individuals of some species respond to local ecological changes by altering the age at which they change sex, although the critical ecological changes appear to be different. The physiological switch that activates sex change also appears to be different: it is found in the cemtral nervous system of the calyptracean Crepidula fornicata, and actually within the gonads of the patellacean Patella vulgata. Although the taxonomic breadth of studies on sex change is necessarily limited, and many questions remain to be answered, research on the Mollusca has produced a remarkable range of perspectives on sex change - from evolutionary to proximal; further research will benefit greatly from this breadth of knowledge.     

Plant controls on Late Quaternary whole ecosystem structure and function

Plants and animals influence biomass production and nutrient cycling in terrestrial ecosystems; however, their relative importance remains unclear. We assessed the extent to which mega‐herbivore species controlled plant community composition and nutrient cycling, relative to other factors during and after the Late Quaternary extinction event in Britain and Ireland, when two‐thirds of the region's mega‐herbivore species went extinct. Warmer temperatures, plant–soil and plant–plant interactions, and reduced burning contributed to the expansion of woody plants and declining nitrogen availability in our five study ecosystems. Shrub biomass was consistently one of the strongest predictors of ecosystem change, equalling or exceeding the effects of other biotic and abiotic factors. In contrast, there was relatively little evidence for mega‐herbivore control on plant community composition and nitrogen availability. The ability of plants to determine the fate of terrestrial ecosystems during periods of global environmental change may therefore be greater than previously thought.     

INVERTEBRATE‐MEDIATED NUTRIENT LOADING INCREASES GROWTH OF AN INTERTIDAL MACROALGA1

Even in nitrogen‐replete ecosystems, microhabitats exist where local‐scale nutrient limitation occurs. For example, coastal waters of the northeastern Pacific Ocean are characterized by high nitrate concentrations associated with upwelling. However, macroalgae living in high‐zone tide pools on adjacent rocky shores are isolated from this upwelled nitrate for extended periods of time, leading to nutrient limitation. When high‐intertidal pools are isolated during low tide, invertebrate‐excreted ammonium accumulates, providing a potential nitrogen source for macroalgae. I quantified the influence of mussels (Mytilus californianus Conrad) on ammonium accumulation rates in tide pools. I then evaluated the effects of ammonium loading by mussels on nitrogen assimilation and growth rates of Odonthalia floccosa (Esp.) Falkenb., a common red algal inhabitant of pools on northeastern Pacific rocky shores. Odonthalia was grown in artificial tide pool mesocosms in the presence and absence of mussels. Mesocosms were subjected to a simulated tidal cycle mimicking emersion and immersion patterns of high‐intertidal pools on the central Oregon coast. In the presence of mussels, ammonium accumulated more quickly in the mesocosms, resulting in increased rates of nitrogen assimilation into algal tissues. These increased nitrogen assimilation rates were primarily associated with higher growth rates. In mesocosms containing mussels, Odonthalia individuals added 41% more biomass than in mesocosms without mussels. This direct positive effect of mussels on macroalgal biomass represents an often overlooked interaction between macroalgae and invertebrates. In nutrient‐limited microhabitats, such as high‐intertidal pools, invertebrate‐excreted ammonium is likely an important local‐scale contributor to macroalgal productivity.     

Marine reserves demonstrate trophic interactions across habitats

Several infaunal bivalve taxa show patterns of decreased biomass in areas with higher densities of adjacent reef-associated predators (the snapper, Pagrus auratus and rock lobster, Jasus edwardsii). A caging experiment was used to test the hypothesis that patterns observed were caused by predation, using plots seeded with a known initial density of the bivalve Dosinia subrosea to estimate survivorship. The caging experiment was replicated at several sites inside and outside two highly protected marine reserves: predators are significantly more abundant inside these reserves. Survivorship in fully caged, partially caged and open plots were then compared at sites having either low (non reserve) or high (reserve) predator density. The highest rates of survivorship of the bivalve were found in caged plots inside reserves and in all treatments outside reserves. However, inside reserves, open and partially caged treatments exhibited low survivorship. It was possible to specifically attribute much of this mortality to predation by large rock lobsters, due to distinctive marks on the valves of dead D. subrosea. This suggests that predation by large rock lobster could indeed account for the distributional patterns previously documented for certain bivalve populations. Our results illustrate that protection afforded by marine reserves is necessary to investigate how depletion through fishing pressure can change the role of upper-level predators and trophic processes between habitats. Electronic Supplementary Material Supplementary material is available for this article at An erratum to this article can be found at