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.     

Demography, competitive interactions and grazing effects of intertidal limpets in southern New Zealand

Population dynamics and the effects of intraspecific competition on limpet growth and maintenance of bare patches were investigated for the intertidal limpet Cellana ornata (Dillwyn) at a boulder-dominated site and on a rocky platform near Kaikoura (South Island), New Zealand. Distribution and abundance patterns of C. ornata were described in relation to other biota and tidal height. C. ornata occurred almost exclusively in patches devoid of macroalgae, particularly in the mid-tidal zone. Both adult and juvenile limpets were most abundant on the tops of boulders, where their numbers were positively correlated with barnacle cover, which averaged 77%. The size structure and growth patterns of C. ornata were different between populations. Mark-recapture studies showed that the slopes of annual growth increments regressed on initial sizes were similar at both sites but that the annual increments on the platform were about 6 mm greater than on boulders. Growth virtually ceased at 27 mm for limpets at the barnacle-dominated boulder site and at 40 mm at the platform site. Recruiting cohorts had 20% survival on boulders and 37% on the platform during their first year. The largest size classes at both sites had around 57% annual survival. To test the effects of varying limpet densities on the growth and mortality of limpets and the maintenance of bare patches, densities of C. ornata were experimentally increased at both sites. Beyond a density of 4 per 0.25 m², sizes and survival of limpets were reduced at both sites, but the effect was more pronounced at the boulder site. Limpets at the boulder site were more effective at maintaining bare space than those on the reef platform. Enclosing limpets in plots with and without barnacles showed that C. ornata and a co-occurring species (Cellana denticulata (Martyn)) grazed more effectively and had greater growth in cleared plots. Overall, there was considerable variation in the demographics of C. ornata between populations driven by site-specific characteristics.     

Top-down impact through a bottom-up mechanism: the effect of limpet grazing on growth,productivity and carbon allocation of Zostera marina L. (eelgrass)

The unusual appearance of a commensal eelgrass limpet [Tectura depicta (Berry)] from southern California at high density (up to 10 shoot^–1) has coincided with the catastrophic decline of a subtidal Zostera marina L. meadow in Monterey Bay, California. Some commensal limpets graze the chloroplast-rich epidermis of eelgrass leaves, but were not known to affect seagrass growth or productivity. We evaluated the effect on eelgrass productivity of grazing by limpets maintained at natural densities (8±2 shoot^–1) in a natural light mesocosm for 45 days. Growth rates, carbon reserves, root proliferation and net photosynthesis of grazed plants were 50–80% below those of ungrazed plants, but biomass-specific respiration was unaffected. The daily period of irradiance-saturated photosynthesis (H _sat) needed to maintain positive carbon balance in grazed plants approached 13.5 h, compared with 5–6 h for ungrazed plants. The amount of carbon allocated to roots of ungrazed plants was 800% higher than for grazed plants. By grazing the chlorophyll-rich epidermis, T. depicta induced carbon limitation in eelgrass growing in an other-wise light-replete environment. Continued northward movement of T. depicta, may have significant impacts on eelgrass production and population dynamics in the northeast Pacific, even thought this limpet consumes very little plant biomass. This interaction is a dramatic example of top-down control (grazing/predation) of eelgrass productivity and survival operating via a bottom-up mechanism (photosynthesis limitation).     

Morphological and molecular tools in identifying the Mediterranean limpets Patella caerulea, Patella aspera and Patella rustica

Allozyme electrophoresis, a partial nucleotide sequence of a mitochondrial gene for cytochrome oxidase I (COI) and discriminant analysis of shell morphometric characters were used to study the relationships among the Sicilian marine gastropods of the Patella genus. Allozyme and mtDNA markers unequivocally distinguished the species and were very useful markers in correctly classifying the different species when morphological characters overlapped each other. Several allozyme loci and many nucleotide positions were diagnostic of species. In contrast, the discriminant analysis of simple morphometric shell characters failed to adequately discriminate the species, suggesting that environmental factors influence colouration and morphological patterns in the Patella species. Our results underline the importance of a genetic approach, as compared to a morphological approach, in discriminating the Mediterranean Patella species.     

Mechanisms and consequences of competition between an alien mussel, Mytilus galloprovincialis, and an indigenous limpet, Scutellastra argenvillei

The influence of an alien mussel Mytilus galloprovincialis (Lamarck) on an indigenous limpet Scutellastra argenvillei (Krauss) was investigated on the west coast of South Africa by comparing four situations in which limpets occupied rock patches surrounded by mussels: (1) ‘established patches’ of high-density adult limpets; (2) ‘experimentally cleared patches’ from which mussels were manually removed; (3) ‘naturally disturbed patches’ where mussels had been eliminated by wave action; and (4) ‘half-density’ patches formed by thinning established patches. Limpets in established patches were most effective in retarding settlement and lateral invasion by mussels, but all patches shrank due to mussel encroachment. As patches shrank, limpet density fell in established and naturally disturbed patches due to emigration. Limpets living on mussel beds were small, sparse and never achieved sexual maturity; 60% shifted to rock, whereas only 7% moved from rock to mussels. The limpets showed highest fidelity to established patches (79% after 12 months) and lowest fidelity in naturally disturbed patches (20%). Thinning of established patches reduced fidelity to 26%. Mussel beds did not provide a suitable alternative substratum for S. argenvillei after they displaced the limpets from rocks. Moreover, elimination of mussels by waves failed to allow S. argenvillei to re-establish dense, adult populations resembling those prior to arrival of the mussel. Adults of S. argenvillei feed collectively by trapping kelp blades. On the topographically complex mussel beds limpets cannot feed this way. In sum, on exposed shores where M. galloprovincialis achieves maximal recruitment and growth, S. argenvillei is incapable of preventing mussel encroachment and is likely to become completely displaced. Semi-exposed shores do, however, offer a refuge preventing global extinction of the limpet.     

Intraspecific interactions between adults and juveniles of the subtidal limpet,Patelloida mufria

Summary Regular monitoring of populations of the subtidal limpet Patelloida mufria (Hedley), which were at naturally large densities (>1000/m²), showed that at the times when there were peaks in juvenile recruitment, the mortality of adults increased greatly. This produced a cyclical pattern in the density of adults, suggesting the juveniles play a partial regulatory role. Experimental manipulations were done to test the influence of overall density and the density of juveniles on the growth and survival of adults. These indicated that an increase in overall density reduced the rate of growth of individuals and increased the rate of adult mortality during the peaks in juvenile recruitment. Similarly, removing these juveniles as they recruited averted this decline in adult abundance. The proposed mechanism to explain these results is that the juveniles have a competitive advantage over adults as they are much smaller and therefore require less energy to survive. It is hypothesisied, therefore, that there will be a threshold of adult size below which the recruits will lose their competitive advantage. Furthermore, if their density became too great, the cover of crustose algae (which is the main food of this species) would be removed resulting in a rapid decline in the numbers of P. mufria. Such an occurrence could be the ultimate regulatory agent for this species.     

Community stability: effects of limpet removal and reintroduction in a rocky intertidal community

Summary The stability of a high rocky intertidal community was assessed in a controlled field experiment in which the most common consumers, limpets, were temporarily removed. Compared to the unmanipulated plots, the exclusion plots developed greater algal abundance and altered species composition of both algae and barnacles. The community was not perturbed beyond its capacity to recover, since the community structure of the limpet-removal plots converged on the structure of the unmanipulated plots following limpet reintroduction. Different components of the community recovered at different rates, depending on whether or not the species had a size-related escape from the limpets. Algae had no size-related escape from limpets. The difference in algal abundance between manipulated and unmanipulated plots lasted less than six months after limpet reintroduction. Barnacles, however, had a size-related escape from limpets and therefore recovered more slowly. The difference in barnacle species composition between the perturbed and unperturbed plots lasted for 17 months after limpet reintroduction. The length of the limpet removal period (16 or 28 months) did not appear to affect the rate of community recovery.     

Metabolic rate depression in a marine pulmonate snail: pre-adaptation for a terrestrial existence?

Summary Terrestrial and freshwater pulmonate snails exhibit a marked depression of aerobic metabolism during estivation. This is an adaptation for existence in periodically harsh environments and, though marine gastropods may undergo anaerobic metabolism, they have not been shown to adaptively depress aerobic metabolic rate. We compared the metabolic response to progressive aerial exposure of two intertidal gastropod limpets, a prosobranch and a pulmonate. The prosobranch Patella granularis maintained a constant heart rate until shortly before death. In contrast, the pulmonate Siphonaria oculus underwent facultative depression of heart rate, accompanied by a decline in oxygen consumption. Both heart rate and oxygen consumption returned to normal levels on reimmersion in water. Metabolic rate depression is energy conserving, and may account for the ability of S. oculus to extend higher up the shore than P. granularis, into areas where food availability is low. S. oculus is a primitive, marine pulmonate, periodically subject to harsh conditions, and its capacity for metabolic rate depression may represent a pre-adaptation for life on land.     

Effects of competition on an endangered limpet Patella ferruginea (Gastropoda: Patellidae): Implications for conservation

Spatial and trophic competitive interactions were analysed for the seldom-studied limpet Patella ferruginea (which is considered as an “extinction risk”). Spatial patterns of distribution of P. ferruginea were studied using quadrats of 1 × 1 m² at several transects along the coastline, whereas trophic interactions were studied through manipulations of densities of P. ferruginea and Patella caerulea in experimental plots located at the mid-shore. Physical parameters were measured inside each plot to determine the microenvironmental differences between fenced and unfenced plots. Fenced plots of 50 × 50 cm² were used with six different treatments. Mortality was recorded every 15 days and length was measured monthly during the 3.5 months of the experiment. At the beginning and end of the experiment, lengths and weights of limpets were recorded and chlorophyll concentration was measured by spectrophotometric analysis of rock surface. Both species showed increased mortality and reduced size and weight in treatments with greater densities. High intraspecific competition was detected in P. caerulea compared with P. ferruginea whereas asymmetrical interspecific competition was observed. The results suggest that P. caerulea is the superior competitor, possibly due to differences in radular morphology and mobility between the two species. Microalgal food assessment showed that it is probably a limiting resource, especially for P. caerulea, although this species has a lower biomass than P. ferruginea. The high intraspecific competition observed in P. caerulea could be responsible for the coexistence of both species. The present study may be useful in helping to conserve P. ferruginea, which is presently under serious threat of extinction, because the results show that experimental fences are a viable means of concentrating breeding individuals.     

Shell alterations in the limpet Bostrycapulus odites: A bioindicator of harbour pollution and mine residuals

Molluscs are commonly used as bioindicators because of their abundance, low motility and the information their shells record. Although in harbour areas gastropod shell deposition would be affected at an endocrinal level, which may increase their vulnerability, studies on the shell of gastropods are scarce. Bostrycapulus odites is a limpet species that possess those characteristics as well as a wide distribution. Limpets were collected in 2001 and 2011, in a channel polluted by both, harbour activities and leaching mine residuals, to compare to a 2011 sample from an unpolluted area within San Antonio Bay. The sensitivity to pollution of this species and the possibility of it use to detect changes in the environmental situation of an area in a 10 years period were investigated. Soft body wet weight and shell morphological variables were measured while shells were also analyzed through scanning electron microscopy and energy dispersive spectroscopy for microstructure and elemental composition, respectively. Maximum likelihood ratio test showed shells from the polluted channel were thicker as well as the same shells presented microstructure malformations and changes in elemental composition (lower Ca and O levels, higher C and Fe levels). The present results indicate that B. odites can be considered a useful bioindicator species to study these kinds of pollution and the potential processes implicated in shell alterations are discussed.