Field experiments with “cageless” methods to manipulate grazing gastropods on intertidal rocky shores

Excluding particular species or guilds of grazing gastropods from experimental areas on intertidal rocky shores is a manipulation frequently used by marine ecologists. Manual removals, cages or fences are classical methods, but they usually require large areas or multiple procedural controls to avoid experimental artefacts. In order to minimise some of those constraints, alternative methods have been developed and are increasingly being used. The effects and limitations of these methods are, however, generally assumed and hardly ever tested. The experiment described here was designed to compare the effectiveness of manual removals, copper paint and sticky barriers in excluding intertidal grazing gastropods from experimental areas on a natural sandstone platform in South-eastern Australia. The response of the grazing assemblage was evaluated for individual species and collectively (integrating all species) by direct counts of individuals and from radular marks on wax discs. The observed patterns varied considerably among species. As predicted, barriers of copper paint effectively excluded the limpet Cellana tramoserica, for several weeks, while having no apparent effect on co-occurring species of grazing gastropods. Sticky barriers were also effective in excluding C. tramoserica, but for shorter periods of time. Contrary to expectations, however, sticky barriers were generally incapable of deterring the coiled snails Bembicium nanum and Nerita atramentosa. Barriers of copper paint are, therefore, a cost-effective way to manipulate diversity (densities of individuals, number and composition of species) and function (intensity of grazing) in this type of assemblage. Care must be taken to clarify the underlying mechanisms and to identify adequate procedural controls.     

Spatial analyses of intertidal assemblages on sheltered rocky shores

Abstract Understanding processes in complex assemblages depends on good understanding of spatial and temporal patterns of structure at various spatial scales. There has been little quantitative information about spatial patterns and natural temporal changes in intertidal assemblages on sheltered rocky shores in temperate Australia. Natural changes and responses to anthropogenic disturbances in these habitats cannot be accurately measured and assessed without quantitative data on patterns of natural variability in space and through time. This paper describes some suitable quantitative methods for examining spatial and temporal patterns of diversity and abundances of highshore, midshore and lowshore intertidal assemblages and the important component species for a number of shores in a bay that has not been severely altered by human disturbance. Despite a diverse flora and fauna on these shores, the midshore and lowshore assemblages on sheltered shores were characterized by a few species which were also the most important in discriminating among assemblages on a shore and, for each assemblage, among different shores. The same set of species was also important for measuring small-scale patchiness within each assemblage (i.e. between replicate sites on a shore). Therefore, these data provide a rationale for selecting species that are useful for measuring differences and changes in abundance among places and times at different scales and, hence, can be used in the more complex sampling designs necessary to detect environmental impacts. There was considerable spatial variability in all assemblages and all species (or taxa) examined at scales of metres, tens of metres and kilometres. There were no clear seasonal trends for most measures, with as much or more variability at intervals of 3 months as from year to year. Most interactions between spatial and temporal measures were at the smallest scale, with different sites on the same shore generally showing different changes from time to time. The cause(s) of this apparently idiosyncratic variability1 were not examined, but some potential causes are discussed. These data are appropriate for testing hypotheses about the applicability of these findings to other relatively undisturbed sheltered shores, about effects of different anthropogenic disturbances on sheltered intertidal assemblages and to test hypotheses about differences in intertidal assemblages on sheltered versus wave-exposed shores.     

Divergent succession and implications for alternative states on rocky intertidal shores

It has been hypothesized that rockweed stands and mussel beds in sheltered bays in the Gulf of Maine, USA, are alternative community states. As a test of this hypothesis, experimental clearings of different sizes were established in stands of the rockweed Ascophyllum nodosum (L.) Le Jolis to determine if successional changes in large clearings developed species assemblages distinctly different from the surrounding A. nodosum stands. Clearings ranging from 1 to 8 m in diameter were created at 12 sites in 4 bays on Swan's Island, Maine, in 1996 to mimic the effects of ice scour, and abundances of gastropods, barnacles, mussels and fucoid algae were monitored until 2002. ANOVAs and MDS showed strong effects of clearing size and divergent successional changes in large clearings. Large clearings were quickly filled in and remained dominated by the alga Fucus vesiculosus L. and the barnacle Semibalanus balanoides (L). There was no evidence for site-specific effects, and Mantel tests showed clearing size was a better predictor of species composition than geographic distances among sites. Results suggest that large pulse disturbances using clearings of 8 m in diameter can initiate divergent successional pathways and have a protracted effect on species composition. Results are also consistent with the hypothesis that mussel beds and rockweed stands in sheltered bays may be alternative community states.     

Using patterns of variability to test for multiple community states on rocky intertidal shores

Predictions based on theory of multiple stable states suggest that larger perturbations should lead to more unpredictable patterns of succession. This prediction was tested in the Gulf of Maine using data from 60 intertidal plots of varying size that were experimentally cleared of the rockweed Ascophyllum nodosum and from 14 benchmark sites from throughout the Gulf. Rockweed was removed from the experimental clearings ranging from 1 to 8 m in diameter in 1996 and data collected in 2004 were used to test effects of clearing size and location on divergence and variability in species composition. Benchmark data were collected in 2005, and the 14 sites were from a dataset on 53 sites throughout the Gulf of Maine. The selected sites were randomly chosen from all sites with > 80% canopy cover by A. nodosum and were expected to be similar to uncleared control plots from the experiment. Experimental removal of A. nodosum resulted in clearings at 12 sites within 4 bays. Abundances of gastropods, barnacles, mussels, and fucoid algae and the percentage cover of barnacles, mussels, fucoid algae, bare space, and other species were sampled. CAP and PERMDISP analyses revealed significant differences in multivariate dispersion and variability with both clearing size and location. Variability generally increased with clearing size and location effects were related to the north-south positioning of the sites. Benchmark sites were similar to the experimental control plots but as variable as the largest clearings. Results suggest that succession in larger clearings has been more unpredictable than in small clearings. The pattern of variability in the experimental clearings is consistent with the predictions of multiple stable states. However, the large amount of variation among the benchmark sites was due to mussels and was unexpected. This unexpected variability underscores the importance of sampling benchmark sites as part of experiments.     

Ability of invertebrate indices to assess ecological condition on intertidal rocky shores

The implementation of directives such as the European Water Framework Directive (WFD) and the Marine Strategy Framework Directive (MSFD) has promoted the development of several tools and methods for assessing the ecological health of marine ecosystems. Within the scope of the WFD and in terms of rocky shores, several multimetric tools were developed based on the macroalgae biological quality element (BQE), in addition to those based on macroinvertebrates.The WFD requires member states to assess each BQE separately. The present work aimed to test the ability of ecological indices to distinguish sites within anthropogenic disturbance gradients caused by organic enrichment, using macroinvertebrate communities on intertidal rocky shores. Owing to the lack of more specific indices (for rocky shore), indices based on abundance, diversity and/or taxonomic composition were selected from several widely used indices in ecological studies and/or developed for soft-bottom macroinvertebrate communities.Present findings reveal several indices based on diversity and/or taxonomic composition able to distinguish sites within the disturbance gradients, showing increasing quality from the site nearest the source of organic enrichment to that farthest from it, especially indices calculated using biomass data, and in the summer season. Such results open good perspectives for the use of intertidal macroinvertebrate communities from rocky shores, and also help add the perspective of this biological quality element in the ecological quality assessment of coastal waters.     

A continental scale evaluation of the role of limpet grazing on rocky shores

It is critical for our knowledge of biodiversity and ecosystem processes to understand how individual species contribute to ecosystem processes and how these contributions vary in space and time. We used a manipulative field experiment in five locations over 17° of latitude [from southern Portugal to the Isle of Man (British Isles)] to determine the relative response of rocky intertidal algal assemblages released from control by the grazing of limpets. Response ratios showed that when limpets were removed there was a trend of effects from north to south. In the north, grazing had a strong effect on algal assemblages, but removing grazers reduced spatial variability in assemblages. In the south, the effect of limpet grazing was far weaker and removal of grazers had a much reduced impact on spatial variability. Here we show a clear trophic control of an ecosystem in that grazing by limpets not only determines macroalgal abundance overall but also modifies ecosystem stability via variability in cover of algae.     

Patterns of spatial variation of assemblages associated with intertidal rocky shores: a global perspective

Assemblages associated with intertidal rocky shores were examined for large scale distribution patterns with specific emphasis on identifying latitudinal trends of species richness and taxonomic distinctiveness. Seventy-two sites distributed around the globe were evaluated following the standardized sampling protocol of the Census of Marine Life NaGISA project (www.nagisa.coml.org). There were no clear patterns of standardized estimators of species richness along latitudinal gradients or among Large Marine Ecosystems (LMEs); however, a strong latitudinal gradient in taxonomic composition (i.e., proportion of different taxonomic groups in a given sample) was observed. Environmental variables related to natural influences were strongly related to the distribution patterns of the assemblages on the LME scale, particularly photoperiod, sea surface temperature (SST) and rainfall. In contrast, no environmental variables directly associated with human influences (with the exception of the inorganic pollution index) were related to assemblage patterns among LMEs. Correlations of the natural assemblages with either latitudinal gradients or environmental variables were equally strong suggesting that neither neutral models nor models based solely on environmental variables sufficiently explain spatial variation of these assemblages at a global scale. Despite the data shortcomings in this study (e.g., unbalanced sample distribution), we show the importance of generating biological global databases for the use in large-scale diversity comparisons of rocky intertidal assemblages to stimulate continued sampling and analyses.     

The grazing effect of limpets on the macroalgal community of a rocky intertidal shore

Abstract Abundance of macro-algae in the mid-littoral zone on a Victorian intertidal rocky shore varied seasonally, algae being rare in Summer and common in Winter and Spring. Field experiments demonstrated that, of two species of grazing limpets (Cellana tramoserica and Siphonana diemenensis), only Siphonaria had a major effect on the abundance of foliose algae (e.g. Scytopsiphon lomeniarid) and neither species had a great effect on the encrusting algae (Ralfsia spp.). There was no evidence of competition for food between the two species of limpets, in contrast with results found for similar species in New South Wales.     

Effects of body size and water temperature on grazing rates of four intertidal gastropods

Abstract Rates of radular activity were measured in four species of Australian gastropods. The species were Austrocochlea constricta, Bembicium nanum, Cellana tramoserica, and Nerita atramentosa. Work was done in Botany Bay at Cape Banks, NSW, Australia from September 1989 to June 1990. A hydrophone was used to record radular raspings of snails in situ. Averages based on all observations showed Cellana had the fastest rate with 80 rasps/min, and was followed by Austrocochlea (71 rasps/min), Bembicium (57), and Nerita (39). Faster rates were associated with warmer water temperature and smaller body sizes in all species except Bembicium. The potential for these differences in radular activity affecting competitive interactions is discussed.     

Molluscan grazing and macroalgal zonation on a rocky intertidal platform at Perth,Western Australia

Abstract Intertidal limestone platforms off Perth show a characteristic pattern of algal zonation, with dense macroalgal beds nearshore bounded by a ‘barren zone’ along the seaward edge. Abalone (Haliotis roei) and several species of limpets and chitons are abundant in the barren zone, which is generally devoid of non-coralline macroalgae. The relative importance of abalone versus limpets and chitons in limiting macroalgal abundance in the barren zone was evaluated by manipulating the presence of each group in a factorial experiment. Percentage algal cover was measured photographically in 0.25m² plots at 1–2 month intervals for 9 months. Mean algal cover (mainly the foliose green alga, Ulva rigida) was highest in plots where all grazers were excluded (77–99%), intermediate where only limpets and chitons were excluded (37–85%), and lowest where only abalone were excluded (4–30%) or where no grazers were excluded (2–19%). The effect of limpets and chitons accounted for 55–89% of the variance in total algal cover, whereas the effect of abalone generally accounted for <10% of the variance. Similar results were obtained in terms of the biomass of Ulva rigida at the end of the experiment. Haliotis roei are relatively large and sedentary herbivores, feeding mainly on drift algae. Their effect on algal abundance was mediated both through pre-emption of space, which might otherwise be colonized by algae, and by grazing around their home scar. Limpets and chitons are smaller than abalone, but were much more abundant. Intensive grazing of the reef surface by limpets and chitons precluded the establishment of non-coralline macroalgae, even where abalone were absent.     

Effects of interactions between algae and grazing gastropods on the structure of a low-shore intertidal algal community

Summary At low levels on shores in New South Wales, foliose algae are abundant and often occupy all substrata; microalgal grazing gastropods are rare or absent. At higher levels, foliose algae are sparse or absent and grazing gastropods are abundant. Hypotheses for the causes of the lower vertical limits of distribution of these grazers include the effects of increased predation or the deleterious physiological effects of increased period of submergence at lower levels on the shore. Alternatively, the presence of the algae, because they occupy space and deprive the grazers of substratum for feeding, may prevent the downward movement, or survival of the grazers at low levels. Under the first two of these hypotheses, algae are able to colonize and grow in low-shore areas as an indirect result of factors which remove grazers. Under the third hypothesis, the algae are directly responsible for the lack of grazers.Experimental clearings of the low-shore algae and introductions of the mid-shore limpets Cellana tramoserica and Siphonaria denticulata were used to test these hypotheses. C. tramoserica grazes microalgae and removes them from the substratum, preventing colonization. S. denticulata, in contrust, crops the algae, leaving a visible cover of algae on the substratum, which can grow rapidly. Because of its method of feeding, S. denticulata had no measurable impact on the rates of colonization, nor on the dry weights of algae, compared with those of ungrazed areas. C. tramoserica could keep cleared areas tree from foliose algae, but only when the limpets were mainfained in great density (10 per 900 cm²). They were less effective where wave-action was greater.Neither species of limpets could survive when placed onto beds of mature algae, because they had no substratum on which to cling and were swept away by the waves. C. tramoserica did not invade clearings below their lower limit of distribution where they had to move over a bed of foliose algae. Few C. tramoserica moved directly downshore into cleared areas. When placed on bare rock within low-shore beds of algae of different ages, S. denticulata remained amongst the algae and maintained their tissue-weights. Few C. tramoserica remained in areas with well-developed algae, compared with areas having sparse algal growth. Those Cellana which remained amongst well-developed algae lost weight, whereas limpets in areas with less algal growth mammtained their weights. In experimental cages in low-shore beds of algae, where the limpets were inaccessible to potential predators, C. tramoserica lost weight and died. On cleared areas they survived for many weeks, but lost weight and died as algae grew and covered the substratum. In the absence of predation, the micro-algal grazer C. tramoserica could not survive in lowshore areas because algae grew too fast and occupied the substratum, making it inaccessible for the limpets to graze; the algae, once grown beyond small sporelings, are not a suitable food-source for C. tramoserica, and the loss of weight and death of these limpets is attributable to starvation.The lower limit of distribution of C. tramoserica is not due to the direct effects of physical factors associated with prolonged submersion, nor to the impact of predators, but is apparently determined by the presence of rapidly growing, extensive beds of foliose algae at low levels on the shore. The cause of the limit of distribution of S. denticulata is not yet known and predation may prove to be important. Removal of S. denticulata from low-shore algal beds would not, however, affect the domination of substrata by algae. Grazing by S. denticulata at very great density had no effect on algal cover nor weight. In the intertidal community studied, the persistence of a low-shore algal zone, bounded above by abundant grazers is not influenced by the activities of predators, but is a direct result of interactions between the grazers and the algae.     

Interactive effects of grazing and enrichment on diversity; conceptual implications of a rocky intertidal experiment

Understanding the ways in which consumers and productivity act and interact to yield differences in diversity is of primary conceptual and pragmatic importance in a world in which humans are simultaneously changing ecological communities and substantially altering the availability of nutrients. Here, I used macroalgal communities on rocky reefs to examine the effects of both limpet grazing and nutrient enrichment on algal diversity throughout almost two years of succession. The experimental design included three levels each of grazing and nutrients, with unglazed terracotta pots attached to the rock as replicate plots in a high intertidal limpet-macroalgal community. Grazing effects varied by year. During the first year, grazing effects were context-dependent with limpets resulting in lower species richness, especially at the highest level of limpet density. However, at this highest level of limpet density, high enrichment counteracted the negative effect of limpets such that diversity was similar to that in treatments with lower limpet densities. In the second year, grazing generally decreased richness, regardless of enrichment. The results of this experiment are partially consistent with the grazer-reversal hypothesis – grazing decreased richness in low nutrient conditions and this effect was neutralized (rather than reversed) under high enrichment. Inconsistencies with model predictions may be explained by the apparent unresponsiveness of algal productivity to experimental enrichment, the unique substrate-scraping feeding mechanisms of limpets, and potentially limited propagule supply.     

Anthropogenic impacts and historical decline in body size of rocky intertidal gastropods in southern California

Abstract The diverse fauna and flora of rocky intertidal ecosystems are being impacted by the activities of rapidly increasing coastal populations in many regions of the world. Human harvesting of intertidal species can lead to significant changes in body sizes of these taxa. However, little is known about the temporal trajectories of such size declines and more importantly, the long‐term effects of chronic human impacts. Furthermore, it is unclear whether sizes of species not directly targeted for harvesting are also declining through indirect effects. Here we use historical (extending back to 1869) and field survey data covering 200 km of mainland southern California coast to show that human activities have led to significant and widespread declines in body sizes of rocky intertidal gastropod species over the last century. These declines, initiated several decades ago, are continuing and contrary to expectation, they are not restricted to species harvested for human consumption. Data from the only national park in this area, where conservation laws are strictly imposed, demonstrate that negative ecological impacts can be ameliorated if existing laws are enforced.     

Observations on Aepophilus bonnairei (Signoret) (Saldidae: Hemiptera) an intertidal insect of rocky shores

Morphological adaptations of the littoral hemipteran Aepophilus bonnairei Sign, to its environment are examined. Particular emphasis is paid to the distribution of the plastron formed by microtrichia and structures around the thoracic spiracles.     

Biotic zonation on rocky shores of Heard Island

Summary The zonation of rocky shore biota on Heard Island is described for the first time, related to a universal zonation scheme and compared with that recorded for other sub-Antarctic localities. The Kelp Zone of holdfasts of the giant kelp, Durvillea antarctica (Chamisso) Hariot (one of the characteristic features of these regions) is confirmed as a sublittoral fringe. The occurrence of a Bare Zone within the littoral zone on sub-Antarctic shores is discussed. The possible roles of submersion, spray, freezing and predation by gulls in influencing the extent and composition of zones are discussed.     

Larval dispersal dampens population fluctuation and shapes the interspecific spatial distribution patterns of rocky intertidal gastropods

Many marine benthic invertebrates pass through a planktonic larval stage whereas others spend their entire lifetimes in benthic habitats. Recent studies indicate that non‐planktonic species show relatively greater fine‐scale patchiness than do planktonic species, but the underlying mechanisms remain unknown. One hypothesis for such a difference is that larval dispersal enhances the connectivity of populations and buffers population fluctuations and reduces local extinction risk, consequently increasing patch occupancy rate and decreasing spatial patchiness. If this mechanism does indeed play a significant role, then the distribution of non‐planktonic species should be more aggregated – both temporally and spatially – than the distribution of species with a planktonic larval stage. To test this prediction, we compared 1) both the spatial and the temporal abundance–occupancy relationships and 2) both the spatial and the temporal mean–variance relationships of population size across species of rocky intertidal gastropods with differing dispersive traits from the Pacific coast of Japan. We found that, compared to planktonic species, non‐planktonic species exhibited 1) a smaller occupancy rate for any given level of mean population size and 2) greater variations in population size, both spatially and temporally. This suggests that the macroecological patterns observed in this study (i.e. the abundance–occupancy relationships and mean–variance relationships of population size across species) were shaped by the effect of larval dispersal dampening population fluctuation, which works over both space and time. While it has been widely assumed that larval dispersal enhances population fluctuations, larval dispersal may in fact enhance the connectively of populations and buffer population fluctuations and reduce local extinction risks.     

Novel use of digital colour-infrared imagery to test hypotheses about grazing by intertidal herbivorous gastropods

Colour-infrared (CIR) imagery was evaluated for its usefulness to test hypotheses about grazing in the intertidal gastropods Nerita atramentosa (Reeve) and Bembicium nanum (Lamarck). Tiles of natural sandstone were placed onto the shore to accumulate micro-algae for a period of 6 weeks. Then, in the laboratory, three replicate tiles were assigned into each of 6 treatments (Nerita and Bembicum at densities of 3 or 6 animals, plus a control and a control for artifacts due to cages). CIR images were acquired before and three times after the animals were placed on the tiles. NIR / red ratio images, which are used to estimate micro-algal biomass, were generated from calibrated CIR data. Nerita at the greater density were more effective at removing micro-algae than at the smaller density. The latter were more effective than Bembicium at either density, which did not significantly decrease algal biomass from that in controls. These data are consistent with previous field observations and indicate that CIR imagery is an effective method for testing hypotheses about grazing by intertidal gastropods.     

Effects of avian grazing on the algal community and small invertebrates in the rocky intertidal zone

In this study of a rocky intertidal habitat in northern Japan, feeding by avian consumers had significant effects on algal assemblages and small herbivorous invertebrates. The effects of the birds on algae were different from those of invertebrate grazers such as urchins and gastropods. The abundance of the dominant algal species decreased during the grazing period, increased again after the grazing period, and indirectly affected algal species richness and evenness. Avian grazing also decreased the density of tube-dwelling amphipods on the dominant alga, but did not change the density of mobile and free-living isopods. These results suggest that avian grazers may act as habitat modifiers rather than exploitative competitors for the small herbivorous crustaceans. Avian herbivores consumed only the upper parts of large algal fronds, apparently reducing the amount of suitable microhabitat for the small herbivorous crustaceans, which are subject to a variety of physical or biological stress. Thus, avian herbivores function as ecosystem engineers, regulating community structure in a manner different to invertebrate herbivores in rocky intertidal habitats.