Interactions between wave action and grazing control the distribution of intertidal macroalgae

Canopy-forming macroalgae are key species on temperate rocky shores. However, there is a lack of understanding of how the relative balance of physical and biological factors controls the establishment and persistence of intertidal macroalgae. Here we present an integrated study of the relative importance of wave-induced forces and grazing for the recruitment and survival of the canopy-forming intertidal macroalgae Fucus vesiculosus and F. spiralis. A set of overtopped breakwaters provided a nearly unconfounded gradient in wave exposure between seaward and landward sides. A biomechanical analysis was performed based on empirical measurements of maximum drag forces in breaking waves, a model of long-term maximum wave height, and the breaking stress of Fucus spp. The estimated maximum flow speed (7-8 m/s) on the seaward side of the breakwaters was predicted to completely dislodge or prune Fucus spp. larger than approximately 10 cm, while dislodgment was highly unlikely on the landward side for all sizes. Experimental transplantation of Fucus spp. supported the biomechanical analysis but also suggested that mechanical abrasion may further limit survival in wave-exposed locations. Experimental removal of the limpet Patella vulgata, which was the principal grazer at this site, resulted in recruitment of Fucus spp. on the seaward side. We present a model of limpet grazing that indicates that limpet densities >5-20 individuals/m2 provide a proximate mechanism preventing establishment of Fucus spp., whereas wave action >2 m/s reduces persistence through dislodgment and battering. In a conceptual model we further propose that recruitment and survival of juvenile Fucus spp. are controlled indirectly by wave exposure through higher limpet densities at exposed locations. This model predicts that climate change, and in particular an increased frequency of storm events in the northeast Atlantic, will restrict fucoids to more sheltered locations.     

Effects of detrital non-native and native macroalgae on the nitrogen and carbon cycling in intertidal sediments

The decay of non-native and native seaweed mixing may modify sediment biogeochemistry and organic matter transfers within benthic food webs according to their composition and biomass. The non-native species Sargassum muticum was deliberately added to the sediment of an intertidal sandflat at different biomass and mixed to the native species Ulva sp. and Fucus vesiculosus. The sediment porewater was then ¹³C and ¹⁵N enriched to test whether both detrital diversity and biomass influenced the transfer of porewater carbon and nitrogen to the sediment and to the macrofauna consumers. More ¹⁵N-nitrogen was mobilized to sediments and macrofauna when the 3-species detrital mixing was buried, probably because this mixing provided species-specific compounds such as polyphenols due to the presence of S. muticum and F. vesiculosus, as well as large amounts of nitrogen due to the presence of Ulva. Our study revealed the importance of detrital diversity and non-native seaweeds for the nitrogen cycling in the benthic food web.     

Effects of wave-induced lightflecks in the intertidal zone on photosynthesis in the macroalgae Postelsia palmaeformis and Hedophyllum sessile (Phaeophyceae)

Intertidal algae are exposed to a highly variable photic regime because of crashing waves. We measured photosynthetic rate of whole fronds of the seaweeds Postelsia palmaeformis (Ruprecht) (at Bodega Marine Laboratory, 1991) and Hedophyllum sessile (Setchell) (Phaeophyceae) (at Friday Harbor Laboratories, 1990) in flashing and steady-state photosynthetically active radiation (PAR) of equal irradiance, using a recirculating metabolism chamber designed to minimize the thickness of diffusional boundary layers on the surfaces of algal tissues. The dimensionless ratio of photosynthetic rate under flecking PAR (P_fleck) and the sum of photosynthetic rate under steady state PAR (P_s) of high and low irradiance was computed for lightfleck periods from 0.2 to 100 s. P_fleck:P_s is a measure of the light-flash utilization-efficiency in flashing light, and was greater than unity at periods between lighflecks of 2 to 30 s, with a peak at 10 s. We used a novel optical fiber irradiance meter to measure PAR incident on fronds of P. palmaeformis as they were washed about by waves breaking in the intertidal zone, and compared the light records to that obtained by a stationary sensor under the canopy. PAR flashing period was closely correlated with the period of breaking waves in stands of P. palmaeformis. We estimated the seasonal spectrum of period between light flashes in stands of this species by examining the spectral density of ocean waves at Bodega Marine Laboratory, Bodega Bay, California. The wave spectrum peaks at a period (10 s) where light-flashes may theoretically enhance the light-flash utilization-efficiency of seaweeds. We calculate that the enhanced light-flash utilization-efficiency wrought by wave-induced light-flashes may contribute to significant gains in primary productivity of these macroalgae under some conditions.     

The seasonal selection by temperature of heterotrophic bacteria in an intertidal sediment

The seasonal selection by temperature of bacteria in an intertidal sediment was investigated, and a simplified method of demonstrating the temperature adaption of a mixed heterotrophic bacterial population was suggested. The method relied upon counting the bacteria which grew at only two separate incubation-temperatures, and compared favourably with more tedions methods which utilise replicated cultures grown at a large number of incubation temperatures. Using this technique, a temperature adaptation index was calculated for the heterotrophic bacterial population and changes in the value of this index were shown to be correlated with seasonal changes of environmental temperature.     

Short- and long-term effects of eutrophication on the secondary production of an intertidal macrobenthic community

Secondary production of a macrobenthic community at an intertidal mudflat was estimated for 33 successive months. Sampling was carried out along a eutrophication gradient, including non-eutrophied Zostera meadows, an intermediate muddy area, and a strongly eutrophied sand-muddy flat, where macroalgal blooms of Enteromorpha spp. usually occur. The Zostera meadows were always the most productive habitat (145–225 g ash-free dry weight m^–2 year^–1). In the short term, the macroalgal bloom benefited the total estuarine production by enhancing the annual production in the eutrophied area. Nevertheless, our results show that this increase was short lived and in no way sufficient to match the production in the Zostera meadows. In the long term, the present study provides evidence that the disappearance of macrophyte beds, as a result of ongoing eutrophication, constitutes a major threat to the sustainability of the estuarine ecosystem.Communicated by S.A. Poulet, Roscoff     

Estimating the effect of air pollution on road safety using atmospheric temperature inversions

Does air quality influence road safety? We estimate the effect of increased air pollution on the number of road traffic accidents in the United Kingdom between 2009 and 2014. To address concerns of spurious correlation we exploit atmospheric temperature inversions as a source of plausibly exogenous variation in daily air pollution levels. We find an increase of 0.3–0.6% in the number of vehicles involved in accidents per day for each additional 1 μg/m³ of PM_2.5. The finding suggests that less safe roads may present a large and previously overlooked cost of air pollution. The results are robust to a number of specifications and across various sub-samples.     

Coefficient of variation of sea surface temperature (SST) as an indicator of coral bleaching

Coral bleaching has become a major problem on reefs around the world in recent decades. It is believed that mean temperature alone is the primary force driving this ecological phenomenon. We propose that variance in temperature in the short term is just as important as the mean. Thirty years of daily sea surface temperature (SST) data have been collected by the University of Puerto Rico at Mayaguez Marine Laboratory in La Parguera, PR. These data were collated and analyzed initially (by Amos Winter) for their relationship to coral bleaching in this area. We found that the data fell into three categories: high mean temperatures associated with severe bleaching, cooler mean temperatures associated with no bleaching, and years of high SSTs but with no coral bleaching. Here, we examined the relationship between mean temperature during those months in which bleaching occurred, temperature variance (as measured by standard deviation), and coefficient of variation (CV; i.e., SD standardized by the mean). We also derived a critical threshold temperature and level of resolution in time for calculating these statistics to clearly describe the circumstances of bleaching versus non-bleaching events, particularly at marginal bleaching temperatures. These characteristics were compared for the four warmest months of the year (July–October) for four warm bleaching years (1969, 1987, 1990, and 1995), four cool non-bleaching years (1984, 1985, 1986, and 1988), and two warm non-bleaching years (1994 and 2000). No relationship was found between the mean SST and SD in terms of predicting bleaching. The two primary statistics which, in concert, did indicate bleaching, however, were the short-term, biweekly mean temperature and its the associated CV. Bleaching occurs in association with both high temperatures and a high CV. The CV becomes a critical determinant of bleaching only when temperatures are ∼29.1–29.8°C. The warm, non-bleaching years were generally characterized by a CV of < 1.9 and a temperature range between 28.5 and 29.9°C. We conclude that increased mean SSTs alone are not sufficient to induce coral bleaching; a high variance in SST at marginal, lower bleaching temperatures can induce bleaching, and likewise, a low variance of such will not induce bleaching. This variance is most clearly described by the CV.     

Effect of freezing on photosynthesis of intertidal macroalgae: relative tolerance of Chondrus crispus and Mastocarpus stellatus (Rhodophyta)

The effect of freezing on photosynthetic metabolism was studied in the red algae, Chondrus crispus and Mastocarpus stellatus. Plants of both species were collected from the intertidal at Chamberlain or Kresge Point, Maine, USA (43°56N, 69°54W) between February and March 1987. Photosynthetic rates were measured immediately after freezing at-20°C and following recovery periods in seawater. Photosynthesis in C. crispus declined rapidly following freezing, falling to 70% of control values within 1 h and 30% after 3 h exposure. Minimum photosynthetic rates (7 to 9% of controls) occurred following freezing exposures of 12 h or more. Full photosynthetic recovery in C. crispus after 3 h at-20°C required 48 h. Photosynthesis in C. crispus did not fully recover in plants frozen for 6 h or more. In contrast, photosynthesis in M. stellatus was relatively unaffected by freezing exposures of <12 h. Twelve hours or more at-20°C reduced photosynthesis to 55% of controls. Photosynthesis in M. stellatus fully recovered from 24 h at-20°C within 24 h. In both species the reduction of photosynthesis by freezing was associated with damage to the plasma membrane and reduced efficiency of energy transfer from phycobilisomes to chlorophyll a, but did not appear to involve ribulose-1,5-bisphosphate carboxylase oxygenase activity. The freezing tolerance of C. crispus and M. stellatus positively correlates with their respective intertidal distributions, suggesting that freezing may be involved in controlling the distributions of these species on the shore.     

Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. I. Sensitivity of photosynthesis to ultraviolet radiation

Marine macroalgae inhabiting Arctic coastal ecosystems are exposed to pronounced seasonal variations in the radiation regime, including harmful UVB radiation. This study presents the first data on the seasonal changes in the sensitivity of macroalgal photosynthesis towards UV exposure by comparing under-ice, clear-water and turbid-water conditions characteristic for late winter, spring and summer. Various brown (Laminaria saccharina, L. digitata, L. solidungula, Saccorhiza dermatodea, Desmarestia aculeata), red (Palmaria palmata, Devaleraea ramentacea) and one green macroalgal species (Monostroma aff. arcticum) were collected at the same water depth throughout the seasons in the Kongsfjord (Spitsbergen, Svalbard, Norway). Maximum quantum yield (F_v/F_m) and maximum photosynthetic electron transport rates (ETR_max) were determined immediately after collection, after 2 h exposure to artificial UV radiation and after 18 h recovery in dim white light. Photosynthesis of the studied species showed different responses depending on their morpho-functional and physiological characteristics, their life strategies, phenology and depth distribution. Within the genus Laminaria, maximum quantum yield of adult specimens of the deep-water species L. solidungula was most strongly UV sensitive. Adult L. saccharina exhibited a lower UV sensitivity than a 6-month-old specimen. Inhibition of photosynthesis after UV exposure remained at the same level throughout the study period, both in adult L. saccharina and S. dermatodea. However, adult specimens of L. saccharina collected in May showed partial recovery only, whereas photosynthesis of specimens from both species collected later recovered fully. D. aculeata exhibited a remarkable decrease of UV sensitivity during the study period. Photosynthesis of specimens collected under the ice was strongly inhibited by UV, but the degree of inhibition decreased during spring and summer. Concomitantly ETR_max values were low after UV exposure in specimens collected in June, but increased later in the season. P. palmata exhibited a relatively flexible response. Photosynthesis in specimens collected under the ice in June or in turbid water in July/August was relatively strongly inhibited; specimens collected during sunny periods and in clear water in spring showed a much lower degree of photoinhibition after UV exposure. The seasonal pattern of low/high ETR_max values in spring/summer is probably a characteristic of the life strategy of this species. The UV sensitivity of D. ramentacea exhibited a similar seasonal pattern. In M. aff. arcticum, UV sensitivity increased and ETR_max values decreased during the study period, reflecting the life strategy of this annual late winter/spring species. The physiological basis for the seasonal changes in UV sensitivity of photosynthesis is presented in a companion paper (this issue).     

Resource acquisition in two intertidal fucoid seaweeds, Fucus serratus and Himanthalia elongata : seasonal variation and effects of reproductive development

Seasonal variations and the effect of reproductive development on resource acquisition by two intertidal fucoid species, the iteroparous Fucus serratus L. and the semelparous Himanthalia elongata (L.) S. F. Gray were examined. The oxygen-exchange characteristics of vegetative apical tissue of both non-fertile and fertile plants and receptacle tissue were compared at monthly intervals throughout reproductive development. Respiratory rates in non-fertile F. serratus varied seasonally between 1.5 and 8.0 μmol g⁻¹ fresh wt h⁻¹; in fertile plants the receptacle had a significantly lower respiratory rate than the vegetative tissue. The respiratory rate of the vegetative button of fertile H. elongata displayed less seasonal variation and was lower than that of the receptacle, which varied from a maximum of 9.5 μmol g⁻¹ fresh wt h⁻¹ at receptacle initiation in October to a minimum of 2.0 μmol g⁻¹ fresh wt h⁻¹ in February. The maximum photosynthetic rate (P _max) of non-fertile plants of both species did not vary in a distinct seasonal manner (∼60 μmol g⁻¹ fresh wt h⁻¹ for F. serratus and ∼12 μmol g⁻¹ fresh wt h⁻¹ for H. elongata). In fertile plants, the P _max of the receptacle tissue was (∼50% lower in F. serratus, and at its peak three times higher in H. elongata, than that of vegetative tissue. The stable carbon-isotope ratio (δ¹³C) did not differ between different tissue types in F. serratus, but values did vary seasonally, being less negative in the summer than in the winter (−13.5‰ compared to −18‰). The receptacle tissue of H. elongata also displayed a distinct seasonal variation in δ¹³C values (−12‰ in summer, −16‰ in winter), whilst the δ¹³C of the vegetative button did not vary seasonally. The rate of uptake of inorganic nitrogen by the vegetative thallus was lower in H. elongata than in F. serratus. The receptacle tissue of F. serratus had lower uptake rates than the vegetative tissue, whilst the uptake rate by H. elongata receptacle tissue was higher than that of the vegetative button. Received: 14 March 1997 / Accepted: 22 April 1997     

Modelling the effects of green macroalgae blooms on the population dynamics of Cyathura carinata (Crustacea: Isopoda) in an eutrophied estuary

A population dynamics model was developed to simulate the effects of benthic macroalgae blooms (mostly Enteromorpha spp.) on the productivity of Cyathura carinata (Crustacea: Isopoda), a possible keystone species in the benthic communities of the Mondego estuary. The model describes C. carinata population dynamics, as well as the relationships between Enteromorpha biomass, Enteromorpha decaying rates, organic matter content in the sediments and detritus consumption by C. carinata, a detritic feeder. Model results support the idea that seasonal blooms of Enteromorpha determine a significant increase of organic matter content in the sediments, due to macroalgae decay, which initially contributes to enhance C. carinata consumption and growth rates, determining a significant increase in the biomass. Nevertheless, later, following the algae bloom, C. carinata biomass decreases, and reaches its lowest value, close to 0, when the algae crash. This effect is probably related with strong anoxic conditions, especially during night, due to high algal decomposition rates. In accordance with the model, migration of new individuals from adjacent areas must occur in order to recolonise the area affected by the algae bloom. Therefore, it seems reasonable to conclude that macroalgae blooms that are limited in space may favour C. carinata populations, but extensive blooms affecting the whole area of distribution of this species will determine its disappearance.     

Photosynthetic response to temperature and desiccation of the intertidal alga Mastocarpus papillatus

When exposed to air during low tide, intertidal macroalgae experience a terrestrial environment and often encounter extreme levels of heating and desiccation. Two aspects of photosynthesis may be influenced by this increase in temperature and decrease in water content during exposure to air: (1) the rate of aerial photosynthesis itself, and (2) the rate at which aquatic photosynthesis recovers upon immersion in water at high tide. This laboratory study examines the effect of air temperature and desiccation on photosynthesis of the intertidal macroalga Mastocarpus papillatus Kützing. Plants were collected at Hopkins Marine Station, California, USA (36°37N; 121°54W) between July and December 1990. When apical tips were exposed to 15 to 25°C air for 2 h, photosynthesis was rapidly recovered upon reimmersion in seawater. Recovery was delayed, but complete, when tissue was exposed to 30°C air, but did not occur after exposure to 35°C air. Desiccation did not influence either the rate or the ultimate level of recovery upon reimmersion. Photosynthesis in air generally decreased with increasing desication, with no net photosynthesis occurring below 25% relative water content. Net photosynthesis of hydrated thalli increased with air temperature from 15 to 30°C, then decreased at 35°C. Dark respiration of hydrated thalli increased over the entire temperature range. This study indicates that thallus heating and desiccation during periods of exposure to air can potentially influence the total carbon budget of M. papillatus.     

Seasonal changes in the structure of an intertidal community

Quantitative (0.25 m²) samples of macrofaunal (>1.0 mm) invertebrates were taken in each season from one habitat of an intertidal sandbar in the North Inlet estuary near Georgetown, South Carolina, USA. During all seasons the community inhabiting the sample site was numerically dominated by two species of haustoriid amphipods (Acanthohaustorius millsi and Pseudohaustorius caroliniensis). Seasonal changes at the community level were clearly controlled by the population dynamics of the numerically dominant species, and qualitative information on life histories was important to the interpretation of analyses' results.This work was supported by the Environmental Technology Center of Martin Marietta Corporation and the Belle W. Baruch Institute for Marine Biology and Coastal Research. It is Contribution No. 138 of the Belle W. Baruch Institute for Marine Biology and Coastal research.     

The Wahlund effect and the geographical scale of variation in the intertidal limpet Siphonaria sp.

Samples of Siphonaria sp. were collected between 1978 and 1982 from sites covering its known geographic range, from Kalbarri, Western Australia to Port Robe, South Australia. Geographic variation of 7 polymorphic enzymes was examined in this intertidal pulmonate limpet, and was found to be consistently small, indicating a large-scale influence of gene flow due to planktonic dispersal. Despite this large-scale uniformity, there is fine-scale genetic patchiness, which is repeated, rather than accumulated, on the larger scale. Throughout its geographic range, Siphonaria sp. shows deficits of heterozygotes for all 7 loci. The consistency among loci indicates that the causes of the deficits are populational, rather than locus-specific. A Wahlund effect, the departure from Hardy-Weinberg equilibrium due to mixing of individuals from groups with different allelic frequencies, is the simplest explanation of such deficits. The limited geographic variation of allelic frequencies, however, is grossly inadequate to produce these deficits through a Wahlund effect. Similarly, temporal variation in allelic frequencies in recruits does not explain the deficits. The largest contributor to a Wahlund effect appears to be binomial sampling variance among small local breeding groups. Thus, mixing of larvae on a scale of metres, rather than among geographical areas, apparently produces the deficits of heterozygotes.     

Testing the effects of wave exposure,site, and behavior on intertidal mussel body temperatures: applications and limits of temperature logger design

The rocky intertidal mussel Mytilus californianus is exposed to potentially damaging thermal conditions during low tide. However, because the temperatures of ectothermic organisms are driven by multiple climatic factors, we do not fully understand what the body temperatures of intertidal invertebrates are under field conditions, or how thermal stress varies between intertidal sites. We designed a temperature logger that thermally matches (similar size, color, morphology and thermal inertia) living mussels of the species M. californianus, and tested its ability to provide realistic measurements of body temperature in the field. As part of these tests, we examined the propensity of M. californianus to gape, a behavior in which the mussel opens its shell valves, and which may permit evaporative cooling. Because our instruments were unable to mimic this behavior, we tested the degree to which gaping contributes to animal cooling by exposing M. californianus to a range of climatic conditions while recording body temperatures, gaping behavior and water loss. Results indicated no significant influence of gaping on body temperature. Tests comparing temperatures of loggers to those of real mussels under laboratory and field conditions showed that thermally matched loggers recorded temperatures within a few degrees of living animals and that unmodified loggers regularly incurred errors of up to 14°C. We then deployed a series of thermally matched loggers at two sites in central Oregon (Boiler Bay and Strawberry Hill) previously hypothesized to display site-specific differences in aerial temperature, and at various wave-exposure regimes within each site. Significant differences were demonstrated between sites using a subset of temperature metrics in a multivariate analysis. Yearly peaks in maximum temperature, average daily maximum temperature, and degree hours were useful in discriminating between sites. In 2001, wave-exposed sites at Strawberry Hill displayed fewer degree–hours than wave-protected sites, but an equivalent or greater maximum temperature. In 2002 both of these metrics were significantly lower in wave-exposed sites. Boiler Bay and Strawberry Hill differed in thermal regime, but not in a way that would indicate one was hotter than the other.Communicated by P.W. Sammarco, Chauvin     

Estimating the biogenic enhancement factor of weathering using an inverse viability method

To determine the influence of the biosphere on weathering we use a dynamic model of the global carbon cycle. It takes into account the most important processes for the long-term evolution of the Earth. The model is solved under a slowly changing environment of increasing solar luminosity and volcanic activity and continental area. By comparing the model results for the global average temperature with data derived from δ¹⁸O values from cherts it is possible to quantify the biogenic enhancement factor of weathering. For this purpose a newly developed inverse viability method is applied, which allows for calculating the range of possible biogenic enhancement factors consistent with the data. We find that in the Precambrian the weathering was 5.4 times lower than in the Phanerozoic era. This supports the hypothesis that the Cambrian explosion was caused by a positive feedback between the spread of biosphere, increased silicate weathering, and a consequent cooling of the climate.     

Sublethal effects of chronic oil exposure on the intertidal clam Macoma balthica

When exposed to Prudhoe Bay crude oil in flowing seawater for 180 days, the small intertidal clam Macoma balthica showed behavioral, physical, physiological and biochemical changes. At a high concentration of oil in seawater (3.0 mg l^-1) burrowing rate decreased, respiration rate increased, growth was inhibited, and very high mortalities resulted. The lowest concentration of oil in seawater (0.03 mg l^-1) inhibited growth and caused reabsorption of gametes. One group of adverse oil effects which was related to sluggishness and disorientation of the clams appeared after a week of exposure to oil; another group related to a negative energy balance was not observed until 60 days. We conclude that chronic exposure of M. balthica to oil-in-seawater concentrations even as low as 0.03 mg l^-1 will, in time, lead to population decreases.Please address requests for reprints to Dr. D. G. Shaw at the Institute of Marine Science