A sixth‐level habitat cascade increases biodiversity in an intertidal estuary

Many studies have documented habitat cascades where two co‐occurring habitat‐forming species control biodiversity. However, more than two habitat‐formers could theoretically co‐occur. We here documented a sixth‐level habitat cascade from the Avon‐Heathcote Estuary, New Zealand, by correlating counts of attached inhabitants to the size and accumulated biomass of their biogenic hosts. These data revealed predictable sequences of habitat‐formation (=attachment space). First, the bivalve Austrovenus provided habitat for green seaweeds (Ulva) that provided habitat for trochid snails in a typical estuarine habitat cascade. However, the trochids also provided habitat for the nonnative bryozoan Conopeum that provided habitat for the red seaweed Gigartina that provided habitat for more trochids, thereby resetting the sequence of the habitat cascade, theoretically in perpetuity. Austrovenus is here the basal habitat‐former that controls this “long” cascade. The strength of facilitation increased with seaweed frond size, accumulated seaweed biomass, accumulated shell biomass but less with shell size. We also found that Ulva attached to all habitat‐formers, trochids attached to Ulva and Gigartina, and Conopeum and Gigartina predominately attached to trochids. These “affinities” for different habitat‐forming species probably reflect species‐specific traits of juveniles and adults. Finally, manipulative experiments confirmed that the amount of seaweed and trochids was important and consistent regulators of the habitat cascade in different estuarine environments. We also interpreted this cascade as a habitat‐formation network that describes the likelihood of an inhabitant being found attached to a specific habitat‐former. We conclude that the strength of the cascade increased with the amount of higher‐order habitat‐formers, with differences in form and function between higher and lower‐order habitat‐formers, and with the affinity of inhabitants for higher‐order habitat‐formers. We suggest that long habitat cascades are common where species traits allow for physical attachment to other species, such as in marine benthic systems and old forest.     

Cost of chemical defence in the red alga Delisea pulchra

The concept of a cost of defence is fundamental to theories for the evolution of defences against consumers. However, the evidence for a cost of plant chemical defences is mixed, and often indirect. This is particularly true for marine macroalgae (seaweeds), for which inferences of cost to date rely almost exclusively on phenotypic correlations between one class of secondary metabolites (brown algal phlorotannins) and growth (or, in one instance, fecundity). No studies of the cost of seaweed chemical defense have experimentally manipulated the presence of secondary metabolites in a controlled fashion and only one previous study has considered genetic background as a factor. Here we measured the cost of halogenated furanones to the red seaweed Delisea pulchra in three ways: a) phenotypic correlations between concentrations of furanones and fecundity in field collected thalli; b) genetic correlations between concentrations of furanones and growth for clones of thalli grown from tetraspores, and c) by comparing growth rates of thalli for which furanone production was experimentally inhibited (furanone -) vs thalli which produced furanones (furanone +). Two of our three tests-correlations between furanones and fecundity, and the growth of furanone (+) vs furanone (−) thalli-indicated a cost of furanones to D. pulchra but genetic correlations between furanones and growth did not. We suggest that these apparently conflicting results are consistent with the consequences of apical growth in this alga, and may further result from a cost of furanones only being manifested at critical developmental stages or times of tissue differentiation.     

Competition induces allelopathy but suppresses growth and anti-herbivore defence in a chemically rich seaweed

Many seaweeds and terrestrial plants induce chemical defences in response to herbivory, but whether they induce chemical defences against competitors (allelopathy) remains poorly understood. We evaluated whether two tropical seaweeds induce allelopathy in response to competition with a reef-building coral. We also assessed the effects of competition on seaweed growth and seaweed chemical defence against herbivores. Following 8 days of competition with the coral Porites cylindrica, the chemically rich seaweed Galaxaura filamentosa induced increased allelochemicals and became nearly twice as damaging to the coral. However, it also experienced significantly reduced growth and increased palatability to herbivores (because of reduced chemical defences). Under the same conditions, the seaweed Sargassum polycystum did not induce allelopathy and did not experience a change in growth or palatability. This is the first demonstration of induced allelopathy in a seaweed, or of competitors reducing seaweed chemical defences against herbivores. Our results suggest that the chemical ecology of coral–seaweed–herbivore interactions can be complex and nuanced, highlighting the need to incorporate greater ecological complexity into the study of chemical defence.     

Characterization of fatty acid composition in healthy and bleached corals from Okinawa, Japan

Under bleaching conditions, corals lose their symbiotic zooxanthellae, and thus, the ability to synthesize fatty acids (FAs) from photosynthetically derived carbon. This study investigated the lipid content and FA composition in healthy and bleached corals from the Odo reef flat in Okinawa, southern Japan, following a bleaching event. It was hypothesized that the FA composition and abundance would change as algae are lost or die, and possibly microbial abundance would increase in corals as a consequence of bleaching. The lipid content and FA composition of three healthy coral species (Pavona frondifera, Acropora pulchra, and Goniastrea aspera) and of partially bleached and completely bleached colonies of P. frondifera were examined. The FA composition did not differ among healthy corals, but differed significantly among healthy, partially bleached, and completely bleached specimens of P. frondifera. Completely bleached corals contained significantly lower lipid and total FA content, as well as lower relative amounts of polyunsaturated FAs and higher relative amounts of saturated FAs, than healthy and partially bleached corals. Furthermore, there was a significantly higher relative concentration of monounsaturated FAs and odd-numbered branched FAs in completely bleached corals, indicating an increase in bacterial colonization in the bleached corals.     

CHEMICAL MEDIATION OF COLONIZATION OF SEAWEED SURFACES1

The surfaces of macroalgal thalli are colonized by planktonic propagules (larvae, spores, cells, etc.) from a wide diversity of eukaryotes and prokaryotes. Colonization (here defined broadly to include processes such as settlement, attachment, metamorphosis, biofilm formation, and infection) of seaweed surfaces can be both induced and inhibited by metabolites produced at those surfaces. However, detailed examples of chemically mediated interactions at seaweed surfaces for which chemical cues have been characterized, quantified in situ, a biological effect determined, and the consequences to the demography of the seaweeds or colonizers demonstrated are very rare. Here we briefly review the literature on both deterrents (“natural antifoulants”) and inducers of colonization and on interactions at seaweed surfaces between the hosts and associated bacterial biofilms. One theme that emerges is the strong need to integrate ecology, cell biology, and chemistry to understand the distribution of surface‐active molecules in situ and their ecological consequences. This multidisciplinary approach is further emphasized for research on biofilms on seaweeds, where recently developed molecular tools for characterizing bacterial communities are opening up an entire new area of marine chemical ecology. Finally, we emphasize an integrated approach to the topic, as we believe that many aspects of somewhat disparate fields including, for example, induction of larval settlement, algal pathogenesis, and the molecular biology of bacterial signaling can be usefully viewed within the overall framework of chemical mediation of surface colonization.     

Does restoration of a habitat‐forming seaweed restore associated faunal diversity?

Declines of habitat‐forming organisms in terrestrial and marine systems can lead to changes in community‐wide biodiversity. The dominant habitat‐forming macroalga Phyllospora comosa (Fucales) went locally extinct along the metropolitan coastline of Sydney in the 1980s. However, the consequences of that disappearance to the associated faunal diversity in these habitats, and whether Phyllospora is ecologically redundant with respect to the biodiversity it supports, are not known. Efforts are underway to restore Phyllospora, and the capacity to enhance local biodiversity is an important component of the rationale for restoration. We compared epifaunal diversity (abundances and composition) between Phyllospora and two other co‐occurring habitat‐forming algae, the kelp Ecklonia radiata and the fucoid Sargassum vestitum, and determined whether Phyllospora transplanted to Sydney developed different epifaunal communities than undisturbed thalli and controls. Where the 3 species naturally co‐occurred, Phyllospora supported different abundances of taxa than Ecklonia and Sargassum, as well as different composition at finer scales, which suggests that this species is not completely redundant and that its disappearance may have affected local biodiversity. Similarly, assemblages on transplanted Phyllospora differed from those on Ecklonia and Sargassum at restored sites, but did not always resemble assemblages from extant natural Phyllospora populations, even 18 months after transplantation. These experiments indicate that restoration of key habitat‐forming seaweeds not only recovers the algal species but also reduces risks of losing habitat diversity for epifauna and their consumers. However, restoration of all the original biodiversity associated with these seaweeds can be a difficult, complex, and long‐term process.     

The future of the northeast Atlantic benthic flora in a high CO2 world

Seaweed and seagrass communities in the northeast Atlantic have been profoundly impacted by humans, and the rate of change is accelerating rapidly due to runaway CO₂ emissions and mounting pressures on coastlines associated with human population growth and increased consumption of finite resources. Here, we predict how rapid warming and acidification are likely to affect benthic flora and coastal ecosystems of the northeast Atlantic in this century, based on global evidence from the literature as interpreted by the collective knowledge of the authorship. We predict that warming will kill off kelp forests in the south and that ocean acidification will remove maerl habitat in the north. Seagrasses will proliferate, and associated epiphytes switch from calcified algae to diatoms and filamentous species. Invasive species will thrive in niches liberated by loss of native species and spread via exponential development of artificial marine structures. Combined impacts of seawater warming, ocean acidification, and increased storminess may replace structurally diverse seaweed canopies, with associated calcified and noncalcified flora, with simple habitats dominated by noncalcified, turf‐forming seaweeds.     

Temperature indirectly affects benthic microalgal diversity by altering effects of top–down but not bottom–up control

Understanding the ecological mechanisms that underlie species diversity decline in response to environmental change has become an urgent objective in current ecological research. Not only direct (lethal) effects on single species but also indirect effects altering biotic interactions between species within and across trophic levels comprise the driving force of ecosystem change. In an experimental marine benthic microalgae–grazer system we tested for indirect effects of moderate temperature change on algal diversity by manipulation of temperature, nutrient supply and grazer density. In our model system warming did not exert indirect effects on microalgal diversity via effects on resource competition. However, moderate warming strengthened consumer control and thereby indirectly affected algal community structure which ultimately resulted in decreased diversity. Only in low temperature and low nutrient regimes did the antagonizing mechanisms of bottom–up and top–down regulation establish a balancing effect on algal diversity within 29 days (corresponding to 15–29 algae generations). Effects of thermal habitat change did not appear before 9–18 algae generations, which points to the relevance of longer‐term experiments and ecological monitoring in order to separate transient biotic responses and subtle changes of community dynamics in consequence to global change.     

Extract powder from the brown alga Ascophyllum nodosum (Linnaeus) Le Jolis (AMPEP): a “vaccine-like” effect on Kappaphycus alvarezii (Doty) Doty ex P.C. Silva

The benefits of using Acadian Marine Plant Extract Powder (AMPEP), obtained from the brown algae Ascophyllum nodosum, for improving growth of the red alga Kappaphycus alvarezii has been demonstrated by authors in the Philippines and Brazil, particularly for increasing daily growth rate and mitigation of epiphytes. However, the processes which occur have not been discussed. This study examined in vitro the relationship between those red algal defense mechanisms and K. alvarezii responses using AMPEP treatments. The administration of the extract reduced the effects of the oxidative burst (production of hydrogen peroxide) which may be extremely aggressive for an individual and its epiphyte. The bleaching of the non-corticated portions of Polysiphonia subtilissima thalli that were cultivated as simulated epiphytes with AMPEP samples confirmed that the reaction was evident in which AMPEP protected K. alvarezii from the hydrogen peroxide effects. It is proposed that the use of the brown seaweed powder AMPEP acts as a potential vaccine, eliciting activation of the red seaweed K. alvarezii natural defenses against pathogens and ameliorating the negative effects of long-term exposure to oxidative bursts.     

The fate of the Arctic seaweed Fucus distichus under climate change: an ecological niche modeling approach

Rising temperatures are predicted to melt all perennial ice cover in the Arctic by the end of this century, thus opening up suitable habitat for temperate and subarctic species. Canopy‐forming seaweeds provide an ideal system to predict the potential impact of climate‐change on rocky‐shore ecosystems, given their direct dependence on temperature and their key role in the ecological system. Our primary objective was to predict the climate‐change induced range‐shift of Fucus distichus, the dominant canopy‐forming macroalga in the Arctic and subarctic rocky intertidal. More specifically, we asked: which Arctic/subarctic and cold‐temperate shores of the northern hemisphere will display the greatest distributional change of F. distichus and how will this affect niche overlap with seaweeds from temperate regions? We used the program MAXENT to develop correlative ecological niche models with dominant range‐limiting factors and 169 occurrence records. Using three climate‐change scenarios, we projected habitat suitability of F. distichus – and its niche overlap with three dominant temperate macroalgae – until year 2200. Maximum sea surface temperature was identified as the most important factor in limiting the fundamental niche of F. distichus. Rising temperatures were predicted to have low impact on the species' southern distribution limits, but to shift its northern distribution limits poleward into the high Arctic. In cold‐temperate to subarctic regions, new areas of niche overlap were predicted between F. distichus and intertidal macroalgae immigrating from the south. While climate‐change threatens intertidal seaweeds in warm‐temperate regions, seaweed meadows will likely flourish in the Arctic intertidal. Although this enriches biodiversity and opens up new seaweed‐harvesting grounds, it will also trigger unpredictable changes in the structure and functioning of the Arctic intertidal ecosystem.     

Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga

Host-pathogen interactions have been widely studied in humans and terrestrial plants, but are much less well explored in marine systems. Here we show that a marine macroalga, Delisea pulchra, utilizes a chemical defence - furanones - to inhibit colonization and infection by a novel bacterial pathogen, Ruegeria sp. R11, and that infection by R11 is temperature dependent. Ruegeria sp. R11 formed biofilms, invaded and bleached furanone-free, but not furanone-producing D. pulchra thalli, at high (24°C) but not low (19°C) temperatures. Bleaching is commonly observed in natural populations of D. pulchra near Sydney, Australia, during the austral summer when ocean temperatures are at their peak and the chemical defences of the alga are reduced. Furanones, produced by D. pulchra as a chemical defence, inhibit quorum sensing (QS) in bacteria, and this may play a role in furanone inhibition of R11 infection of furanone-free thalli as R11 produces QS signals. This interplay between temperature, an algal chemical defence mechanism and bacterial virulence demonstrates the complex impact environmental change can have on an ecosystem.     

Mesoherbivores reduce net growth and induce chemical resistance in natural seaweed populations

Herbivory on marine macroalgae (seaweeds) in temperate areas is often dominated by relatively small gastropods and crustaceans (mesoherbivores). The effects of these herbivores on the performance of adult seaweeds have so far been almost exclusively investigated under artificial laboratory conditions. Furthermore, several recent laboratory studies with mesoherbivores indicate that inducible chemical resistance may be as common in seaweeds as in vascular plants. However, in order to further explore and test the possible ecological significance of induced chemical resistance in temperate seaweeds, data are needed that address this issue in natural populations. We investigated the effect of grazing by littorinid herbivorous snails (Littorina spp.) on the individual net growth of the brown seaweed Ascophyllum nodosum in natural field populations. Furthermore, the capacity for induced resistance in the seaweeds was assessed by removing herbivores and assaying for relaxation of defences. We found that ambient densities of gastropod herbivores significantly reduced net growth by 45% in natural field populations of A. nodosum. Seaweeds previously exposed to grazing in the field were less consumed by gastropod herbivores in feeding bioassays. Furthermore, the concentration of phlorotannins (polyphenolics), which have been shown to deter gastropod herbivores, was higher in the seaweeds that were exposed to gastropod herbivores in the field. This field study corroborates earlier laboratory experiments and demonstrates that it is important to make sure that the lack of experimental field data on marine mesoherbivory does not lead to rash conclusions about the lack of significant effects of these herbivores on seaweed performance. The results strongly suggest that gastropods exert a significant selection pressure on the evolution of defensive traits in the seaweeds, and that brown seaweeds can respond to attacks by natural densities of these herbivores through increased chemical resistance to further grazing.     

Arctic marine phytobenthos of northern Baffin Island

Global climate change is expected to alter the polar bioregions faster than any other marine environment. This study assesses the biodiversity of seaweeds and associated eukaryotic pathogens of an established study site in northern Baffin Island (72° N), providing a baseline inventory for future work assessing impacts of the currently ongoing changes in the Arctic marine environment. A total of 33 Phaeophyceae, 24 Rhodophyceae, 2 Chlorophyceae, 12 Ulvophyceae, 1 Trebouxiophyceae, and 1 Dinophyceae are reported, based on collections of an expedition to the area in 2009, complemented by unpublished records of Robert T. Wilce and the first‐ever photographic documentation of the phytobenthos of the American Arctic. Molecular barcoding of isolates raised from incubated substratum samples revealed the presence of 20 species of brown seaweeds, including gametophytes of kelp and of a previously unsequenced Desmarestia closely related to D. viridis, two species of Pylaiella, the kelp endophyte Laminariocolax aecidioides and 11 previously unsequenced species of the Ectocarpales, highlighting the necessity to include molecular techniques for fully unraveling cryptic algal diversity. This study also includes the first records of Eurychasma dicksonii, a eukaryotic pathogen affecting seaweeds, from the American Arctic. Overall, this study provides both the most accurate inventory of seaweed diversity of the northern Baffin Island region to date and can be used as an important basis to understand diversity changes with climate change.     

Stressor intensity determines antagonistic interactions between species invasion and multiple stressor effects on ecosystem functioning

Biological invasions, nutrient enrichment and ocean warming are known to threaten biodiversity and ecosystem functioning. The independent effects of these ecological stressors are well studied, however, we lack understanding of their cumulative effects, which may be additive, antagonistic or synergistic. For example, the impacts of biological invasions are often determined by environmental context, which suggests that the effects of invasive species may vary with other stressors such as pollution or climate change. This study examined the effects of an invasive seaweed (Sargassum muticum) on the structure and functioning of a synthetic macroalgal assemblage and tested explicitly whether these effects varied with nutrient enrichment and ocean warming. Overall, the presence of S. muticum increased assemblage productivity rates and warming altered algal assemblage structure, which was characterised by a decrease in kelp and an increase in ephemeral green algae. The effects of S. muticum on total algal biomass accumulation, however, varied with nutrient enrichment and warming, producing antagonistic cumulative effects on total algal biomass accumulation. These findings show that the nature of stressor interactions may vary with stressor intensity and among response variables, which leads to less predictable consequences for the structure and functioning of communities.     

Detrimental effects of host anemone bleaching on anemonefish populations

Coral bleaching and related reef degradation have caused significant declines in the abundance of reef-associated fishes. Most attention on the effects of bleaching has focused on corals, but bleaching is also prevalent in other cnidarians, including sea anemones. The consequences of anemone bleaching are unknown, and the demographic effects of bleaching on associated fish recruitment, survival, and reproduction are poorly understood. We examined the effect of habitat degradation including host anemone bleaching on fish abundance, egg production, and recruitment of the panda anemonefish (Amphiprion polymnus) near Port Moresby, Papua New Guinea. Following a high-temperature anomaly in shallow waters of the region, most shallow anemones to a depth of 6 m (approximately 35% of all the anemones in this area) were severely bleached. Anemone mortality was low but bleached anemones underwent a ~34% reduction in body size. Total numbers of A. polymnus were not affected by bleaching and reduction in shelter area. While egg production of females living in bleached anemones was reduced by ~38% in 2009 compared to 2008, egg production of females on unbleached anemones did not differ significantly between years. Total recruitment in 2009 was much lower than in 2008. However, we found no evidence of recruiting larvae avoiding bleached anemones at settlement suggesting that other factors or different chemical cues were more important in determining recruitment than habitat quality. These results provide the first field evidence of detrimental effects of climate-induced bleaching and habitat degradation on reproduction and recruitment of anemonefish.     

Impact of Menthol on Growth and Photosynthetic Function of Breviolum Minutum (Dinoflagellata,Dinophyceae, Symbiodiniaceae) and Interactions with its Aiptasia Host

Environmental change, including global warming and chemical pollution, can compromise cnidarian‐(e.g., coral‐) dinoflagellate symbioses and cause coral bleaching. Understanding the mechanisms that regulate these symbioses will inform strategies for sustaining healthy coral–reef communities. A model system for corals is the symbiosis between the sea anemone Exaiptasia pallida (common name Aiptasia) and its dinoflagellate partners (family Symbiodiniaceae). To complement existing studies of the interactions between these organisms, we examined the impact of menthol, a reagent often used to render cnidarians aposymbiotic, on the dinoflagellate Breviolum minutum, both in culture and in hospite. In both environments, the growth and photosynthesis of this alga were compromised at either 100 or 300 µM menthol. We observed reduction in PSII and PSI functions, the abundances of reaction‐center proteins, and, at 300 µM menthol, of total cellular proteins. Interestingly, for free‐living algae exposed to 100 µM menthol, an initial decline in growth, photosynthetic activities, pigmentation, and protein abundances reversed after 5–15 d, eventually approaching control levels. This behavior was observed in cells maintained in continuous light, but not in cells experiencing a light–dark regimen, suggesting that B. minutum can detoxify menthol or acclimate and repair damaged photosynthetic complexes in a light‐ and/or energy‐dependent manner. Extended exposures of cultured algae to 300 µM menthol ultimately resulted in algal death. Most symbiotic anemones were also unable to survive this menthol concentration for 30 d. Additionally, cells impaired for photosynthesis by pre‐treatment with 300 µM menthol exhibited reduced efficiency in re‐populating the anemone host.     

RECENT ADVANCES IN FERTILIZATION ECOLOGY OF MACROALGAE1

Our understanding of natural patterns of fertilization in seaweeds has increased substantially over the last 10 years due to new approaches and methods to characterize the nature and frequency of fertilization processes in situ, to recognize the conditions and mechanisms enhancing fertilization success, and to anticipate population and community consequences of the patterns of natural fertilization. Successful reproduction in many species depends on a delicate juxtaposition of abiotic and biotic conditions. Important abiotic factors are those triggering gamete release (e.g. single or interacting effects of light quality and water movement) and those affecting gamete viability or concentrations (e.g. salinity effects on polyspermy blocks; gamete dilution due to water movement). Examples of important biotic components are synchronous gamete release, efficiency of polyspermy‐blocking mechanisms, population density of sexually fertile thalli, interparent distances, and male‐to‐female ratios. Field data indicate fertilization frequencies of 70%–100% in broadcasting‐type seaweeds (e.g. fucoids) and 30%–80% in brooding‐type (red) algae. Red algal values are higher than previously thought and challenge presently accepted explanations for their complex life histories. Important population and community questions raised by the recent findings relate to the magnitude of gene flow and exchange occurring in many micropopulations that seemingly breed during periods of isolation, the physiological basis and population effects of male‐to‐male competition and sexual selection during fertilization of brooding seaweeds, and the effects of massive gamete release, especially in holocarpic seaweeds, on benthic and planktonic communities. Comparative studies in other algal groups are now needed to test the generality of the above patterns, to provide critical pieces of information still missing in our understanding of natural fertilization processes, and to elucidate the evolutionary consequences of the different modes of reproduction (e.g. brooders vs. broadcasters).     

Synergistic effects of temperature and light affect the relationship between Taonia atomaria and its epibacterial community: a controlled conditions study

In the context of global warming, this study aimed to assess the effect of temperature and irradiance on the macroalgal Taonia atomaria holobiont dynamics. We developed an experimental set-up using aquaria supplied by natural seawater with three temperatures combined with three irradiances. The holobiont response was monitored over 14 days using a multi-omics approach coupling algal surface metabolomics and metabarcoding. Both temperature and irradiance appeared to shape the microbiota and the surface metabolome, but with a distinct temporality. Epibacterial community first changed according to temperature, and later in relation to irradiance, while the opposite occurred for the surface metabolome. An increased temperature revealed a decreasing richness of the epiphytic community together with an increase of several bacterial taxa. Irradiance changes appeared to quickly impact surface metabolites production linked with the algal host photosynthesis (e.g. mannitol, fucoxanthin, dimethylsulfoniopropionate), which was hypothesized to explain modifications of the structure of the epiphytic community. Algal host may also directly adapt its surface metabolome to changing temperature with time (e.g. lipids content) and also in response to changing microbiota (e.g. chemical defences). Finally, this study brought new insights highlighting complex direct and indirect responses of seaweeds and their associated microbiota under changing environments.