Consumption rates of the periwinkle Littorina obtusata on the brown seaweed Ascophyllum nodosum

Anti-herbivory defenses support persistence of seaweeds. Little is known, however, about temporal dynamics in the induction of grazer-deterrent seaweed traits. In two induction experiments, consumption rates of the periwinkle Littorina obtusata (L.) on the brown seaweed Ascophyllum nodosum (L.) Le Jolis were measured in 3-d intervals. Changes in palatability of directly grazed A. nodosum were tested every 3 d with feeding assays using fresh and reconstituted seaweed pieces. Likewise, assays with fresh A. nodosum assessed changes in seaweed palatability in response to water-borne cues from nearby grazed conspecifics. Consumption rates of L. obtusata varied significantly during the 27-d induction phase of each experiment. Direct grazing by L. obtusata lowered palatability of fresh and reconstituted A. nodosum pieces to conspecific grazers after 15 d as well as after 6 and 12 d, respectively. After 12, 18, and 24 d, fresh A. nodosum located downstream of L. obtusata-grazed conspecifics was significantly less palatable than A. nodosum located downstream of ungrazed conspecifics. Changes in L. obtusata consumption rates and A. nodosum palatability during both induction experiments suggest temporal variation of grazer-deterrent responses, which may complicate experimental detection of inducible anti-herbivory defenses.

Marine meso-herbivore consumption scales faster with temperature than seaweed primary production, supplementary material

Respiration of ectotherms is predicted to increase faster with rising environmental temperature than photosynthesis of primary producers because of the differential temperature dependent kinetics of the key enzymes involved. Accordingly, if biological processes at higher levels of complexity are constrained by underlying metabolic functions food consumption by heterotrophs should increase more rapidly with rising temperature than photo-autoptrophic primary production. We compared rates of photosynthesis and growth of the benthic seaweed Fucus vesiculosus with respiration and consumption of the isopod Idotea baltica to achieve a mechanistic understanding why warming strengthens marine plant-herbivore interactions. In laboratory experiments thallus pieces of the seaweed and individuals of the grazer were exposed to constant temperatures at a range from 10 to 20°C. Photosynthesis of F. vesiculosus did not vary with temperature indicating efficient thermal acclimation whereas growth of the algae clearly increased with temperature. Respiration and food consumption of I. baltica also increased with temperature. Grazer consumption scaled about 2.5 times faster with temperature than seaweed production. The resulting mismatch between algal production and herbivore consumption may result in a net loss of algal tissue at elevated temperatures. Our study provides an explanation for faster decomposition of seaweeds at elevated temperatures despite the positive effects of high temperatures on algal growth.

Seawater carbonate chemistry, nutrients and growth rate of coral (Acropora intermedia) and coral-reef seaweed (Lobophora papenfussii) during experiments, 2011

Space competition between corals and seaweeds is an important ecological process underlying coral-reef dynamics. Processes promoting seaweed growth and survival, such as herbivore overfishing and eutrophication, can lead to local reef degradation. Here, we present the case that increasing concentrations of atmospheric CO2 may be an additional process driving a shift from corals to seaweeds on reefs. Coral (Acropora intermedia) mortality in contact with a common coral-reef seaweed (Lobophora papenfussii) increased two- to threefold between background CO2 (400 ppm) and highest level projected for late 21st century (1140 ppm). The strong interaction between CO2 and seaweeds on coral mortality was most likely attributable to a chemical competitive mechanism, as control corals with algal mimics showed no mortality. Our results suggest that coral (Acropora) reefs may become increasingly susceptible to seaweed proliferation under ocean acidification, and processes regulating algal abundance (e.g. herbivory) will play an increasingly important role in maintaining coral abundance.

Growth response of an early successional assemblage of coralline algae and benthic diatoms to ocean acidification

The sustained absorption of anthropogenically released atmospheric CO2 by the oceans is modifying seawater carbonate chemistry, a process termed ocean acidification (OA). By the year 2100, the worst case scenario is a decline in the average oceanic surface seawater pH by 0.3 units to 7.75. The changing seawater carbonate chemistry is predicted to negatively affect many marine species, particularly calcifying organisms such as coralline algae, while species such as diatoms and fleshy seaweed are predicted to be little affected or may even benefit from OA. It has been hypothesized in previous work that the direct negative effects imposed on coralline algae, and the direct positive effects on fleshy seaweeds and diatoms under a future high CO2 ocean could result in a reduced ability of corallines to compete with diatoms and fleshy seaweed for space in the future. In a 6-week laboratory experiment, we examined the effect of pH 7.60 (pH predicted to occur due to ocean acidification just beyond the year 2100) compared to pH 8.05 (present day) on the lateral growth rates of an early successional, cold-temperate species assemblage dominated by crustose coralline algae and benthic diatoms. Crustose coralline algae and benthic diatoms maintained positive growth rates in both pH treatments. The growth rates of coralline algae were three times lower at pH 7.60, and a non-significant decline in diatom growth meant that proportions of the two functional groups remained similar over the course of the experiment. Our results do not support our hypothesis that benthic diatoms will outcompete crustose coralline algae under future pH conditions. However, while crustose coralline algae were able to maintain their presence in this benthic rocky reef species assemblage, the reduced growth rates suggest that they will be less capable of recolonizing after disturbance events, which could result in reduced coralline cover under OA conditions.

Seawater carbonate chemistry and giant kelp Macrocystis pyrifera reproduction processes during experiments, 2011

The worldwide effects of ocean acidification (OA) on marine species are a growing concern. In temperate coastal seas, seaweeds are dominant primary producers that create complex habitats and supply energy to higher trophic levels. Studies on OA and macroalgae have focused on calcifying species and adult stages but, critically, they have overlooked the microscopic stages of the reproductive life cycle, which, for other anthropogenic stress e.g. UV-B radiation, are the most susceptible life-history phase. Also, environmental cues and stressors can cause changes in the sex ratio which has implications for the mating system and recruitment success. Here, we report the effects of pH (7.59-8.50) on meiospore germination and sex determination for the giant kelp, Macrocystis pyrifera (Laminariales), in the presence and absence of additional dissolved inorganic carbon (DIC). Lowered pH (7.59-7.60, using HCl-only) caused a significant reduction in germination, while added DIC had the opposite effect, indicating that increased CO2 at lower pH ameliorates physiological stress. This finding also highlights the importance of appropriate manipulation of seawater carbonate chemistry when testing the effects of ocean acidification on photosynthetic organisms. The proportion of male to female gametophytes did not vary significantly between treatments suggesting that pH was not a primary environmental modulator of sex. Relative to the baseline (pH 8.19), gametophytes were 32% larger under moderate OA (pH 7.86) compared to their size (10% increase) under extreme OA (pH 7.61). This study suggests that metabolically-active cells can compensate for the acidification of seawater. This homeostatic function minimises the negative effects of lower pH (high H+ ions) on cellular activity. The 6-9% reduction in germination success under extreme OA suggests that meiospores of M.pyrifera may be resistant to future ocean acidification.

Skeletal trade-offs in coralline algae in response to ocean acidification

Ocean acidification is changing the marine environment, with potentially serious consequences for many organisms. Much of our understanding of ocean acidification effects comes from laboratory experiments, which demonstrate physiological responses over relatively short timescales. Observational studies and, more recently, experimental studies in natural systems suggest that ocean acidification will alter the structure of seaweed communities. Here, we provide a mechanistic understanding of altered competitive dynamics among a group of seaweeds, the crustose coralline algae (CCA). We compare CCA from historical experiments (1981-1997) with specimens from recent, identical experiments (2012) to describe morphological changes over this time period, which coincides with acidification of seawater in the Northeastern Pacific. Traditionally thick species decreased in thickness by a factor of 2.0-2.3, but did not experience a change in internal skeletal metrics. In contrast, traditionally thin species remained approximately the same thickness but reduced their total carbonate tissue by making thinner inter-filament cell walls. These changes represent alternative mechanisms for the reduction of calcium carbonate production in CCA and suggest energetic trade-offs related to the cost of building and maintaining a calcium carbonate skeleton as pH declines. Our classification of stress response by morphological type may be generalizable to CCA at other sites, as well as to other calcifying organisms with species-specific differences in morphological types.

Seawater carbonate chemistry and growth, reproduction of calcifying and non-calcifying epibionts of a brown macroalga in a laboratory experiment

Seaweeds are key species of the Baltic Sea benthic ecosystems. They are the substratum of numerous fouling epibionts like bryozoans and tubeworms. Several of these epibionts bear calcified structures and could be impacted by the high pCO2 events of the late summer upwellings in the Baltic nearshores. Those events are expected to increase in strength and duration with global change and ocean acidification. If calcifying epibionts are impacted by transient acidification as driven by upwelling events, their increasing prevalence could cause a shift of the fouling communities toward fleshy species. The aim of the present study was to test the sensitivity of selected seaweed macrofoulers to transient elevation of pCO2 in their natural microenvironment, i.e. the boundary layer covering the thallus surface of brown seaweeds. Fragments of the macroalga Fucus serratus bearing an epibiotic community composed of the calcifiers Spirorbis spirorbis (Annelida) and Electra pilosa (Bryozoa) and the non-calcifier Alcyonidium hirsutum (Bryozoa) were maintained for 30 days under three pCO2 conditions: natural 460±59 µatm, present-day upwelling1193±166 µatm and future upwelling 3150±446 µatm. Only the highest pCO2 caused a significant reduction of growth rates and settlement of S. spirorbis individuals. Additionally, S. spirorbis settled juveniles exhibited enhanced calcification of 40% during daylight hours compared to dark hours, possibly reflecting a day-night alternation of an acidification-modulating effect by algal photosynthesis as opposed to an acidification-enhancing effect of algal respiration. E. pilosa colonies showed significantly increased growth rates at intermediate pCO2 (1193 µatm) but no response to higher pCO2. No effect of acidification on A. hirsutum colonies growth rates was observed. The results suggest a remarkable resistance of the algal macro-epibionts to levels of acidification occurring at present day upwellings in the Baltic. Only extreme future upwelling conditions impacted the tubeworm S. spirorbis, but not the bryozoans.

Contrasting effects of ocean acidification on tropical fleshy and calcareous algae

Despite the heightened awareness of ocean acidification (OA) effects on marine organisms, few studies empirically juxtapose biological responses to CO2 manipulations across functionally distinct primary producers, particularly benthic algae. Algal responses to OA may vary because increasing CO2 has the potential to fertilize photosynthesis but impair biomineralization. Using a series of repeated experiments on Palmyra Atoll, simulated OA effects were tested across a suite of ecologically important coral reef algae, including five fleshy and six calcareous species. Growth, calcification and photophysiology were measured for each species independently and metrics were combined from each experiment using a meta-analysis to examine overall trends across functional groups categorized as fleshy, upright calcareous, and crustose coralline algae (CCA). The magnitude of the effect of OA on algal growth response varied by species, but the direction was consistent within functional groups. Exposure to OA conditions generally enhanced growth in fleshy macroalgae, reduced net calcification in upright calcareous algae, and caused net dissolution in CCA. Additionally, three of the five fleshy seaweeds tested became reproductive upon exposure to OA conditions. There was no consistent effect of OA on algal photophysiology. Our study provides experimental evidence to support the hypothesis that OA will reduce the ability of calcareous algae to biomineralize. Further, we show that CO2 enrichment either will stimulate population or somatic growth in some species of fleshy macroalgae. Thus, our results suggest that projected OA conditions may favor non-calcifying algae and influence the relative dominance of fleshy macroalgae on reefs, perpetuating or exacerbating existing shifts in reef community structure.

Bicarbonate uptake via an anion exchange protein is the main mechanism of inorganic carbon acquisition by the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) under variable pH

Macrocystis pyrifera is a widely distributed, highly productive, seaweed. It is known to use bicarbonate (HCO3-) from seawater in photosynthesis and the main mechanism of utilization is attributed to the external catalyzed dehydration of HCO3- by the surface-bound enzyme carbonic anhydrase (CAext). Here, we examined other putative HCO3- uptake mechanisms in M. pyrifera under pHT 9.00 (HCO3-: CO2 = 940:1) and pHT 7.65 (HCO3-: CO2 = 51:1). Rates of photosynthesis, and internal CA (CAint) and CAext activity were measured following the application of AZ which inhibits CAext, and DIDS which inhibits a different HCO3- uptake system, via an anion exchange (AE) protein. We found that the main mechanism of HCO3- uptake by M. pyrifera is via an AE protein, regardless of the HCO3-: CO2 ratio, with CAext making little contribution. Inhibiting the AE protein led to a 55%-65% decrease in photosynthetic rates. Inhibiting both the AE protein and CAext at pHT 9.00 led to 80%-100% inhibition of photosynthesis, whereas at pHT 7.65, passive CO2 diffusion supported 33% of photosynthesis. CAint was active at pHT 7.65 and 9.00, and activity was always higher than CAext, because of its role in dehydrating HCO3- to supply CO2 to RuBisCO. Interestingly, the main mechanism of HCO3- uptake in M. pyrifera was different than that in other Laminariales studied (CAext-catalyzed reaction) and we suggest that species-specific knowledge of carbon uptake mechanisms is required in order to elucidate how seaweeds might respond to future changes in HCO3-:CO2 due to ocean acidification.

Experiment: Combined effects of CO2, temperature, irradiance and time on the physiological performance of Chondrus crispus (Rhodophyta)

In natural environments, marine biotas are exposed to a variety of simultaneously acting abiotic factors. Among these, temperature, irradiance and CO2 availability are major factors influencing the physiological performance of marine macroalgae. To test whether elevated levels of CO2 may remediate the otherwise reduced performance of uncalcified seaweeds under the influence of other stressful abiotic factors, we performed multifactorial experiments with the red alga Chondrus crispus from Helgoland (North Sea) with two levels of CO2, temperature and irradiance: low and high pCO2 levels were tested in combination with either (1) optimal and low irradiances or (2) optimal and sub-lethal high temperatures for growth. Performance of C. crispus was evaluated as biomass increase and relative growth rates (RGR), gross photosynthesis and pigment content. Acclimations of growth and photosynthesis were measured after 4 and 8 days. Acclimation time was crucial for elucidating single or combined CO2 effects on growth and photosynthesis. Signifi- cant CO2 effects became evident only in combination with either elevated temperature or reduced irradiance. Growth and photosynthesis had divergent patterns: RGR and biomass significantly increased only under a combination of high pCO2 and elevated temperature; gross photosynthesis was significantly reduced under high pCO2 conditions at low irradiance. Pigment content varied in response to irradiance and temperature, but was independent of pCO2.

The future of coral reefs

Coral reefs, with their millions of species, have changed profoundly because of the effects of people, and will continue to do so for the foreseeable future. Reefs are subject to many of the same processes that affect other human-dominated ecosystems, but some special features merit emphasis: (i) Many dominant reef builders spawn eggs and sperm into the water column, where fertilization occurs. They are thus particularly vulnerable to Allee effects, including potential extinction associated with chronic reproductive failure. (ii) The corals likely to be most resistant to the effects of habitat degradation are small, short-lived “weedy” corals that have limited dispersal capabilities at the larval stage. Habitat degradation, together with habitat fragmentation, will therefore lead to the establishment of genetically isolated clusters of inbreeding corals. (iii) Increases in average sea temperatures by as little as 1°C, a likely result of global climate change, can cause coral “bleaching” (the breakdown of coral–algal symbiosis), changes in symbiont communities, and coral death. (iv) The activities of people near reefs increase both fishing pressure and nutrient inputs. In general, these processes favor more rapidly growing competitors, often fleshy seaweeds, and may also result in explosions of predator populations. (v) Combinations of stress appear to be associated with threshold responses and ecological surprises, including devastating pathogen outbreaks. (vi) The fossil record suggests that corals as a group are more likely to suffer extinctions than some of the groups that associate with them, whose habitat requirements may be less stringent.

Successful external fertilization in turbulent environments.

Mathematical and experimental simulations predict that external fertilization is unsuccessful in habitats characterized by high water motion. A key assumption of such predictions is that gametes are released in hydrodynamic regimes that quickly dilute gametes. We used fucoid seaweeds to examine whether marine organisms in intertidal and subtidal habitats might achieve high levels of fertilization by restricting their release of gametes to calm intervals. Fucus vesiculosus L. (Baltic Sea) released high numbers of gametes only when maximal water velocities were below ca. 0.2 m/s immediately prior to natural periods of release, which occur in early evening in association with lunar cues. Natural fertilization success measured at two sites was always close to 100%. Laboratory experiments confirmed that (i) high water motion inhibits gamete release by F. vesiculosus and by the intertidal fucoids Fucus distichus L. (Maine) and Pelvetia fastigiata (J. Ag.) DeToni (California), and (ii) showed that photosynthesis is required for high gamete release. These data suggest that chemical changes in the boundary layer surrounding adults during photosynthesis and/or mechanosensitive channels may modulate gamete release in response to changing hydrodynamic conditions. Therefore, sensitivity to environmental factors can lead to successful external fertilization, even for species living in turbulent habitats.