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 and bottom-up community regulation in marine rocky intertidal habitats

Strong top-down control by consumers has been demonstrated in rocky intertidal communities around the world. In contrast, the role of bottom-up effects (nutrients and productivity), known to have important influences in terrestrial and particularly freshwater ecosystems, is poorly known in marine hard-bottom communities. Recent studies in South Africa, New England, Oregon and New Zealand suggest that bottom-up processes can have important effects on rocky intertidal community structure. A significant aspect of all of these studies was the incorporation of processes varying on larger spatial scales than previously considered (10’s to 1000’s of km). In all four regions, variation in oceanographic factors (currents, upwelling, nutrients, rates of particle flux) was associated with different magnitudes of algal and/or phytoplankton abundance, availability of particulate food, and rates of recruitment. These processes led to differences in prey abundance and growth, secondary production, consumer growth, and consumer impact on prey resources. Oceanographic conditions therefore may vary on scales that generate ecologically significant variability in populations at the bottom of the food chain, and through upward-flowing food chain effects, lead to variation in top-down trophic effects. I conclude that top-down and bottom-up processes can be important joint determinants of community structure in rocky intertidal habitats, and predict that such effects will occur generally wherever oceanographic ‘discontinuities’ lie adjacent to rocky coastlines. I further argue that increased attention by researchers and of funding agencies to such benthic–pelagic coupling would dramatically enhance our understanding of the dynamics of marine ecosystems.     

A test of the Menge-Sutherland model of community organization in a tropical rocky intertidal food web

Summary Menge and Sutherland (1976) predicted that in physically benign habitats: (1) community structure will be most strongly affected be predation, (2) the effect of predation will increase with a decrease in trophic position in the food web, (3) trophically intermediate species will be influenced by both predation and competition, and (4) competition will occur among prey species which successfully escape consumers. These predictions were tested in a tropical rocky intertidal community on the Pacific coast of Panama. The most abundant mobile species included fishes and crabs, which occupied the top trophic level, and predaceous gastropods and herbivorous molluscs, which occupied intermediate trophic levels. The most abundant sessile organisms were encrusting algae, foliose algae, barnacles, and bivalves. Diets were broad and overlapping, and 30.3% of the consumers were omnivorous. Each consumer group had strong effects on prey occurring at lower trophic levels: (1) Fishes and crabs reduced the abundance of predaceous snails, herbivorous molluscs, foliose algae, and sessile invertebrates. (2) Predaceous gastropods reduced the abundance of herbivorous molluscs and sessile invertebrates. (3) Herbivorous molluscs reduced the abundance of foliose algae and young stages of sessile invertebrates, and altered relative abundances of the encrusting algae. The encrusting algae, although normally the dominant space occupiers, proved to be inferior competitors for space with other sessile organisms when consumers were experimentally excluded. However, the crusts escaped consumers by virtue of superior anti-herbivore defenses and competed for space despite intense grazing. Observations do not support the hypothesis that the trophically intermediate species compete. Hence, with the exception of this last observation, the predictions of the Menge and Sutherland model were supported. Although further work is needed to evaluate other predictions of the model in this community, evidence from this study joins an increasing body of knowledge supporting the model. Contradictory evidence also exists, however, indicating that aspects of the model require revision.     

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.     

Climate-driven interactions among rocky intertidal organisms caught between a rock and a hot place

To explore how climate may affect the structure of natural communities, we quantified the role of thermal stress in setting the high intertidal borders of the acorn barnacle, Semibalanus balanoides. At sites north and south of Cape Cod, a major faunal and thermal boundary on the east coast of North America, we examined the interacting effects of thermal stress and recruit density on individual survivorship. At hotter southern sites, particularly in bays, high intertidal barnacle survivorship was enhanced by experimental shading or by neighbors which ameliorate heat and desiccation stresses. In contrast, at cooler northern bay and coastal sites, neither shading nor group benefits increased barnacle survival, and mortality patterns were driven primarily by predators with largely boreal distributions. Our field results, like recent laboratory microcosm studies, suggest that predicting even simple community responses to climate change may be more complex than is currently appreciated. Received: 26 January 1999 / Accepted: 5 April 1999     

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.     

The structure and replenishment of rocky shore intertidal communities and biogeographic comparisons

Marine scientists have made many recent advances in understanding the connections between the structure of benthic communities, replenishment of populations through dispersal processes, and interactions with the nearshore water mass. In this review, some of the themes and models relating to these processes and interactions are discussed. Benthic–pelagic coupling models are in the early stages of development, but encompass oceanic processes such as upwelling and downwelling, the transport of larvae and their arrival back to shore to settle. Most current knowledge of these processes is based on a few taxa, especially barnacles and mussels. This is discussed with reference and comparison to macroalgae, which dominate much of the intertidal zone on temperate rocky shores, and have quite different life histories, transport and settlement processes. The role of key, habitat-dominating species is discussed, particularly their early life histories, with reference to the differences in community composition, nearshore dynamics and settlement processes in different countries. Finally, some suggestions are made for future work to fill gaps in understanding about rocky shore communities.     

中街山列岛岩相潮间带大型底栖动物的群落格局

于2006年9月和2007年7月在中街山列岛4个有居民海岛岩相潮间带设立8个断面,对大型底栖动物的群落结构进行了调查。共获得大型底栖动物34种,其中腔肠动物1种,环节动物3种,甲壳动物10种,软体动物20种。优势种有日本笠藤壶(Tetraclita japonica)、紫贻贝(Mytilus edulis)和节蝾螺(Turb articulatus)等4种。以季节和站位为因子对多样性指数进行双因素方差分析,结果表明只有夏、秋季丰富度指数(P=0.028)存在显著差异,其他指数的方差分析没有显著差异(P>0.05)。3个潮带4个岛屿共12个站位的聚类分析和MDS标序分析表明,12个群落可分为3组(Ⅰ、Ⅱ和Ⅲ组)。大型底栖动物ABC曲线分析表明底栖动物群落尚未受到干扰。     

An experimental evaluation of the direct and indirect effects of endemic seaweeds,barnacles, and invertebrate predators on the abundance of the introduced rocky intertidal barnacle Balanus glandula

The barnacle, Balanus glandula has recently invaded along the Pacific coast of eastern Hokkaido, Japan. To evaluate the direct and indirect effects of endemic seaweeds, barnacles, and invertebrate predators on the abundance of B. glandula on the rocky intertidal coast of eastern Hokkaido, we conducted a field experiment from June 2011 to October 2012 in which we manipulated the presence or absence of these factors. Seaweeds showed no significant effect on the abundance of B. glandula. The endemic barnacle Chthamalus dalli and the invertebrate predator Nucella lima reduced the abundance of B. glandula. However, the simultaneous influence of N. lima and C. dalli was compensative rather than additive, probably due to keystone predation. These findings suggest that competition by the endemic barnacle C. dalli and predation by the invertebrate predator N. lima decreased the abundance of B. glandula, but that N. lima predation on C. dalli weakened the negative influence of C. dalli on B. glandula. The implications of these findings are twofold: the endemic competitor and invertebrate predator may have played important roles in decreasing the abundance of B. glandula in natural habitats, and conservation of endemic invertebrate predators may be crucial to impede the establishment and survival of introduced barnacles in rocky intertidal habitats.     

Response of a rocky intertidal ecosystem engineer and community dominant to climate change

To evaluate how climate change might impact a competitively dominant ecological engineer, we analysed the growth response of the mussel Mytilus californianus to climate patterns [El Niño-Southern Oscillation, Pacific Decadal Oscillation (PDO)]. Mussels grew faster during warmer climatic events. Growth was initially faster on a more productive cape compared to a less productive cape. Growth rates at the two capes merged in 2002, coincidentally with a several year-long shift from warm to cool PDO conditions. To determine the mechanism underlying this response, we examined growth responses to intertidal sea and air temperatures, phytoplankton, sea level and tide height. Together, water temperature (32%) and food (12.5%) explained 44.5% of the variance in mussel growth; contributions of other factors were not significant. In turn, water temperature and food respond to climate-driven variation in upwelling and other, unknown factors. Understanding responses of ecosystem engineers to climate change will require knowing direct thermal effects and indirect effects of factors altered by temperature change.     

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.     

Anthropogenic harvesting pressure and changes in life history: insights from a rocky intertidal limpet

The importance of large breeding individuals for maintaining the health of marine fish and invertebrate populations has long been recognized. Unfortunately, decades of human harvesting that preferentially remove larger individuals have led to drastic reductions in body sizes of many of these species. Such size-selective harvesting is particularly worrisome for sequentially hermaphroditic species where the larger size classes are composed primarily of one sex. Whether these species can maintain stable sex ratios under sustained harvesting pressure depends on the level of plasticity of their life-history traits. Here, we show that populations of a marine limpet (Lottia gigantea) can adjust a fundamental aspect of their life history (the timing of sex change) when subjected to size-selective harvesting. As predicted by theoretical models, individuals from harvested populations change sex at smaller sizes and grow at slower rates compared to individuals from protected populations. In addition, the relative size at which the change from male to female occurs remains constant (~0.75; size at sex change/maximum size) across populations, regardless of harvesting pressure. Our results show that population-level demographic and life-history data, in conjunction with existing theory, can be sufficient to predict the responses of sequential hermaphrodites to harvesting pressure. Furthermore, they suggest such species can potentially adapt to size-selective harvesting.     

Feeding guild structure of a rocky intertidal fish assemblage in central Chile

The identification and analysis of the guild structure of vertebrate assemblages has played a fundamental role in the understanding of the underlying mechanisms responsible for their community organization and structuring. This approach generally has not been undertaken for temperate water intertidal fish assemblages. In central Chile, fishes are important components of the intertidal community, but no studies attempting to understand their organization and structuring have been done. In the present study, the diets of 13 of the most abundant species which inhabit tidepools in the rocky intertidal zone of central Chile were determined. A total of 660 fishes was collected at 5 sites: Los Molles, Con-Cón, Quintay, El Tabo, and Las Cruces. Dietary overlap between all species pairs was calculated and a phenogram of dietary similarity was constructed and analyzed using a bootstrapping technique to objectively determine guild membership. The results showed that the intertidal fish assemblage of central Chile can be divided into three feeding guilds: two guilds consisting of carnivorous species and one guild of omnivorous and herbivorous species. The possible causes and implications of the resulting guild structure and the potential effects of predation by these fishes on other components of the intertidal community are discussed.     

Sediment on rocky intertidal reefs: Effects on early post-settlement stages of habitat-forming seaweeds

Modification of the coastal environment by human activities often leads to an increase in sedimentation of nearshore waters, with potential impacts on benthic marine assemblages. Here we assess the relationships between the levels of sedimentation, wave exposure and benthic organisms on rocky intertidal platforms around the Kaikoura Peninsula in southern New Zealand. We designed and tested five sediment traps to provide a tool for measuring the relative abundance of sediment across sites. Using field- and laboratory-based experiments, we tested hypotheses concerning whether different levels of sedimentation affected algal germling survival and algal zygote attachment, and whether the interactions of grazers and sediments affected germling survival. Levels of sediment and exposure were inversely related across seven sites. The fucoid alga Hormosira banksii characterized the more sedimented wave-sheltered and intermediately wave-exposed sites, with up to 80% cover in the lower mid-tidal zone, while the bull kelp Durvillaea antarctica characterized the three most wave-exposed sites. Grazing molluscs were found across all sites but species abundances varied by sediment and exposure levels. We did two 11-day trials testing the effects of different levels of sediment and different species of molluscan grazers on the survival of 1-week-old Hormosira germlings. Generally, there was no significant treatment effect of grazers, but mortality varied considerably among sites. In particular, one site had very high levels of sediment, which resulted in 100% mortality of germlings across all grazer treatments. Removing sediment at 1-week, 2-week and 4-week intervals made no difference to the survival of Hormosira germlings. In laboratory-based experiments, a light dusting of sediment reduced the percentage of zygotes of Hormosira by 34% and Durvillaea by 71% that attached to primary substratum, and a complete cover of sediment prevented attachment altogether. Overall, the effects of sediments and its interaction with molluscan grazing were highly variable but often large, particularly on the attachment of zygotes to primary substratum.     

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.     

Predation by gulls on crabs in rocky intertidal and shallow subtidal zones of the Gulf of Maine

Most organisms in intertidal areas are marine in origin; many have distributions that extend into the subtidal zone. Terrestrial predators such as mammals and birds may exploit these animals during low tide and can have considerable effects on intertidal food webs. Several studies have shown that avian predators are capable of reducing densities of sessile and slow-moving intertidal invertebrates but very few studies have considered avian predation on mobile invertebrate predators such as crabs. In this study, we investigated predation by Great Black-backed Gulls (Larus marinus Linnaeus) on three species of crabs (Cancer borealis Stimpson, Cancer irroratus Say, and Carcinus maenas Linnaeus). The study was at Appledore Island, ME (a gull breeding island) and 8 other sites throughout the Gulf of Maine, including breeding islands and mainland sites. On Appledore Island, intertidal and subtidal zones provided over one-third of prey remains found at gull nests, and crabs were a substantial proportion (∼ 30% to 40%) of the total remains. Similarly, collections of prey remains from intertidal areas indicated that crabs were by far the most common marine prey. C. borealis was eaten far more often and C. irroratus and C. maenas less often than expected at each site. Comparing numbers of carapaces to densities of crabs in low intertidal and shallow subtidal zones at each site, we estimated that gulls remove between 15% and 64% of C. borealis during diurnal low tides. The proportion of C. borealis eaten by gulls was independent of proximity to a gull colony. Approximately 97% of the outer coast of Maine is within 20 km of a breeding island. Thus, a lot of gull predation on crabs may occur throughout the Gulf of Maine during summer months. Crabs are important predators of other invertebrates; if predation by gulls reduces the number of crabs in intertidal and shallow subtidal areas, gulls may have important indirect effects on intertidal food webs.     

Thermal constraints on daily patterns of aggregation and density along an intertidal gradient in the periwinkle Echinolittorina peruviana

Variations in environmental temperature have both direct and indirect effects that affect organisms at levels ranging from intra-cellular physiological processes to ecological patterns. These variations are especially important for intertidal marine ectotherms such as littorinids since they alternate between periods of immersion in seawater, and must also experience long periods of emersion. In central Chile, Echinolittorina peruviana is one of the most conspicuous species on rocky intertidal shores, occurring at high tidal levels and in the splash zone. The species is known to resist direct exposure to the sun for long periods, although juveniles tend to be restricted to protected microhabitats. Adults show seasonal variations in abundance and vertical distribution and may form aggregations that have been shown to help reduce water loss and body temperature. In this study, we evaluate the relationship between daily thermal variations throughout the vertical distribution of this species and how these affect the patterns of density and aggregation. Our results suggest that one of the leading determinants of the spatio-temporal variation of density in E. peruviana may be operative temperature (T_O: the amount of stored heat resulting from the balance between heat fluxes into and out of the body, measured with taxidermic mounts mimicking heat transfer properties of the snail). T_O showed a strong negative relationship with density and a strong positive relationship with aggregation in the highest intertidal level monitored. The strength of these relationships decreased in importance at lower levels. While T_O alone cannot explain the abundance of E. peruviana throughout its range of distribution, our results show that it does have a strong influence that should be considered in addition to other ecological factors affecting the density of intertidal littorinids.     

An experimental test of the effects of variation in recruitment intensity on intertidal community composition

The rocky intertidal has been a model system for experimentally testing hypotheses regarding the factors that structure natural communities. Many ecologists have proposed that changes in the intensity of recruitment of individuals into a community should influence community structure. Past work investigating this hypothesis has primarily been surveys of recruitment and community structure across large spatial scales. Surprisingly, no researchers to date have manipulated recruitment into a rocky intertidal community to assess the response of interactions of the whole community to variation in recruitment intensity. We manipulated the densities of Balanus glandula and Chthamalus spp. recruits across a four-fold difference at two sites spanning the Monterey Bay, California, USA, to experimentally test if differences in recruitment intensity influenced initial changes in community composition and if these changes persisted through time. The results of this work indicate that differences in recruitment influence community composition initially, but that these changes can be short-lived.     

Contrasting spatial heterogeneity of sessile organisms within mussel (Perna perna L.) beds in relation to topographic variability

We examined the spatial heterogeneity in three sessile rocky shore organisms, the mussel Perna perna, the barnacle Octomeris angulosa (Sowerby) and the red alga Gelidium pristoides (Turn.) at a range of continuous local scales along horizontal transects within mid- and upper mussel beds of South African shores. We also examined the relationships between variability of organisms and topographic features (rock depressions, slope, aspect), and between mussel, barnacle and algal variability over the same scales. To estimate spatial heterogeneity, we analyzed scaling properties of semivariograms using a fractal approach. Relationships between different variables at the different scales were examined by cross-semivariograms. Spatial dependence of P. perna variability increased with spatial dependence of topographic variability, so that scaling regions of mussel and topographic distributions corresponded well. This relationship often improved with larger local scales (mussel cover increased with depressions, steeper slope and aspect towards waves), while at smaller spatial scales, variability in mussel cover was less well explained by variability in topography. The variability of the barnacle O. angulosa exhibited spatial dependence, even on topographically unstructured shores. In contrast, the distribution of the alga G. pristoides revealed high fractal dimensions, showing spatial independence on topographically unstructured shores. Algae also showed a very strong negative relationship with mussels at most local scales, and a negative relationship with barnacles in upper zones, especially at larger local scales. Barnacles may show clear spatial dependence because of hydrodynamics (at larger local scales) and the need to find a future mate in close proximity (at smaller local scales), while algae may show a strong negative relationship with mussels because of competition for space.