Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems.
TL;DR: How chemical cues regulate critical aspects of the behavior of marine organisms from bacteria to phytoplankton to benthic invertebrates and water column fishes is reviewed.
Abstract: Chemical cues constitute much of the language of life in the sea. Our understanding of biotic interactions and their effects on marine ecosystems will advance more rapidly if this language is studied and understood. Here, I review how chemical cues regulate critical aspects of the behavior of marine organisms from bacteria to phytoplankton to benthic invertebrates and water column fishes. These chemically mediated interactions strongly affect population structure, community organization, and ecosystem function. Chemical cues determine foraging strategies, feeding choices, commensal associations, selection of mates and habitats, competitive interactions, and transfer of energy and nutrients within and among ecosystems. In numerous cases, the indirect effects of chemical signals on behavior have as much or more effect on community structure and function as the direct effects of consumers and pathogens. Chemical cues are critical for understanding marine systems, but their omnipresence and impact are inadequ...
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TL;DR: The present article reviews two decades of research on the red seaweed Delisea pulchra by addressing: the defense chemistry of this seaweed; chemically-mediated interactions between the seaweed and its natural enemies; and the negative influence of elevated seawater temperature on these interactions.
Abstract: The need for animals and plants to control microbial colonization is important in the marine environment with its high densities of microscopic propagules and seawater that provides an ideal medium for their dispersal. In contrast to the traditional emphasis on antagonistic interactions of marine organisms with microbes, emerging studies lend support to the notion that health and performance of many marine organisms are functionally regulated and assisted by associated microbes, an ecological concept defined as a holobiont. While antimicrobial activities of marine secondary metabolites have been studied in great depth ex-situ, we are beginning to understand how some of these compounds function in an ecological context to maintain the performance of marine holobionts. The present article reviews two decades of our research on the red seaweed Delisea pulchra by addressing: the defense chemistry of this seaweed; chemically-mediated interactions between the seaweed and its natural enemies; and the negative influence of elevated seawater temperature on these interactions. Our understanding of these defense compounds and the functional roles they play for D. pulchra extends from molecular interactions with bacterial cell signaling molecules, to ecosystem-scale consequences of chemically-controlled disease and herbivory. Delisea pulchra produces halogenated furanones that antagonize the same receptor as acylated homoserine lactones (AHL)—a group of widespread intercellular communication signals among bacteria. Halogenated furanones compete with and inhibit bacterial cell-to-cell communication, and thus interfere with important bacterial communication-regulated processes, such as biofilm formation. In a predictable pattern that occurs at the ecological level of entire populations, environmental stress interferes with the production of halogenated furanones, causing downstream processes that ultimately result in disease of the algal holobiont.
56 citations
TL;DR: The contributing role chemosensory communication plays in the ability of sponge larvae to identify suitable habitat for successful recruitment is demonstrated and the possibility that larvae from distinct phyla may share signal transduction pathways involved in metamorphosis is raised.
Abstract: In sessile marine invertebrates, larval settlement is fundamental to population maintenance and persistence. Cues contributing to the settlement choices and metamorphosis of larvae have important implications for the success of individuals and populations, but cues mediating larval settlement for many marine invertebrates are largely unknown. This study assessed larval settlement in two common Great Barrier Reef sponges, Coscinoderma matthewsi and Rhopaloeides odorabile, to cues that enhance settlement and metamorphosis in various species of scleractinian coral larvae. Methanol extracts of the crustose coralline algae (CCA), Porolithon onkodes, corresponding to a range of concentrations, were used to determine the settlement responses of sponge larvae. Cnidarian neuropeptides (GLW-amide neuropeptides) were also tested as a settlement cue. Settlement in both sponge species was approximately two-fold higher in response to live chips of CCA and optimum concentrations of CCA extract compared to 0.2 µm filtered sea water controls. Metamorphosis also increased when larvae were exposed to GLW-amide neuropeptides; R. odorabile mean metamorphosis reached 42.0±5.8% compared to 16.0±2.4% in seawater controls and in C. matthewsi mean metamorphosis reached 68.3±5.4% compared to 36.7±3.3% in seawater controls. These results demonstrate the contributing role chemosensory communication plays in the ability of sponge larvae to identify suitable habitat for successful recruitment. It also raises the possibility that larvae from distinct phyla may share signal transduction pathways involved in metamorphosis.
55 citations
Cites background from "Marine chemical ecology: chemical s..."
...Chemical cues are also implicated in larval settlement [12]....
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TL;DR: Marine microbes have the potential as upcoming and promising source of non-toxic compounds with sustainable anti-biofouling/anti- biofilm properties as they can produce substances that can inhibit not only the chemical components required for biofilm production but also the attachment, microorganism growth, and/or cell–cell communication.
Abstract: Natural products from the unique environments of sea water and oceans represent a largely unfamiliar source for isolation of new microbes, which are potent producers of secondary bioactive metabolites. These unique life-forms from the marine ecosphere have served as an important source of drugs since ancient times and still offer a valuable resource for novel findings by providing remedial treatments. Therefore, it can be expected that many naturally bioactive marine microbial compounds with novel structures and bioactivities against those from terrestrial environments may be found among marine metabolites. Biofilms in aquatic environment possess serious problems to naval forces and oceanic industries around the globe. Current anti-biofilm or anti-biofouling technology is based on the use of toxic substances that can be harmful to their surrounding natural locales. Comprehensive research has been done to examine the bioactive potential of marine microbes. Results are remarkably varied and dynamic, but there is an urgent need for bioactive compounds with environmentally friendly or "green" chemical activities. Marine microbes have the potential as upcoming and promising source of non-toxic compounds with sustainable anti-biofouling/anti-biofilm properties as they can produce substances that can inhibit not only the chemical components required for biofilm production but also the attachment, microorganism growth, and/or cell-cell communication.
52 citations
Cites background from "Marine chemical ecology: chemical s..."
...Several other studies have reported the isolation of bioactive metabolites from microorganisms associated with their invertebrate hosts (Kelecom, 2002; Bernan, Greenstein & Maiese, 1997; Hay, 2009)....
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TL;DR: Ascidians maintain secondary metabolic symbioses with bacteria that are phylogenetically diverse, indicating a convergent solution to obtaining secondary metabolites and reinforcing the importance of secondary metabolism in animal survival.
Abstract: Bioactive secondary metabolites are common components of marine animals. In many cases, symbiotic bacteria, and not the animals themselves, synthesize the compounds. Among marine animals, ascidians are good models for understanding these symbioses. Ascidians often contain potently bioactive secondary metabolites as their major extractable components. Strong evidence shows that ~8% of the known secondary metabolites from ascidians are made by symbiotic bacteria, and indirect evidence implicates bacteria in the synthesis of many more. Far from being “secondary” to the animals, secondary metabolites are essential components of the interaction between host animals and their symbiotic bacteria. These interactions have complex underlying biology, but the chemistry is clearly ascidian-species specific. The chemical interactions are ancient in at least some cases, and they are widespread among ascidians. Ascidians maintain secondary metabolic symbioses with bacteria that are phylogenetically diverse, indicating a convergent solution to obtaining secondary metabolites and reinforcing the importance of secondary metabolism in animal survival.
51 citations
TL;DR: A system capable of non-invasively imaging seafloor environments and organisms in situ at nearly micrometre resolution is presented, which can provide important new insights into micro-scale processes in benthic ecosystems that shape observed patterns at much larger scales.
Abstract: Microscopic-scale processes significantly influence benthic marine ecosystems such as coral reefs and kelp forests. Due to the ocean's complex and dynamic nature, it is most informative to study these processes in the natural environment yet it is inherently difficult. Here we present a system capable of non-invasively imaging seafloor environments and organisms in situ at nearly micrometre resolution. We overcome the challenges of underwater microscopy through the use of a long working distance microscopic objective, an electrically tunable lens and focused reflectance illumination. The diver-deployed instrument permits studies of both spatial and temporal processes such as the algal colonization and overgrowth of bleaching corals, as well as coral polyp behaviour and interspecific competition. By enabling in situ observations at previously unattainable scales, this instrument can provide important new insights into micro-scale processes in benthic ecosystems that shape observed patterns at much larger scales.
50 citations
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Journal Article•
839 citations
"Marine chemical ecology: chemical s..." refers background in this paper
...…to chemical cues from specific hosts, or corals that settle in response to chemical traits of specific crustose coralline algae, or of soft-substrate animals that recruit to or avoid sands treated with specific chemical cues or extracts (e.g., Pawlik 1992, Krug & Manzi 1999, Hadfield & Paul 2001)....
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...In aquatic systems, chemical cues determine feeding, habitat, and mating choices (e.g., Hay & Fenical 1988, 1996; Pawlik 1992; Breithaupt & Thiel 2008)....
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...…stimulating feeding once prey have been contacted; compounds responsible for attraction from a distance have rarely been investigated for adult specialist consumers [compounds that cue larval settlement have been investigated; see Pawlik (1992), Krug & Manzi (1999), and Hadfield & Paul (2001)]....
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TL;DR: It is concluded that the best way to protect salt marshes and the services they provide is through the integrated approach of ecosystem-based management.
Abstract: Salt marshes are among the most abundant, fertile, and accessible coastal habitats on earth, and they provide more ecosystem services to coastal populations than any other environment. Since the Middle Ages, humans have manipulated salt marshes at a grand scale, altering species composition, distribution, and ecosystem function. Here, we review historic and contemporary human activities in marsh ecosystems—exploitation of plant products; conversion to farmland, salt works, and urban land; introduction of non-native species; alteration of coastal hydrology; and metal and nutrient pollution. Unexpectedly, diverse types of impacts can have a similar consequence, turning salt marsh food webs upside down, dramatically increasing top down control. Of the various impacts, invasive species, runaway consumer effects, and sea level rise represent the greatest threats to salt marsh ecosystems. We conclude that the best way to protect salt marshes and the services they provide is through the integrated approach of ecosystem-based management.
770 citations
TL;DR: Although numerous seaweed characteristics can deter some herbivores, the effects of morphology and chemistry have been studied most thoroughly and these types of seaweeds may be considered herbivore tolerant.
Abstract: Herbivory has a profound effect on seaweeds in both temperate and tropical communities (11, 17, 21, 33, 43, 47, 80, 124). This is especially true on coral reefs where 60-97% (11, 42) of the total seaweed production may be removed by herbivores. To persist in marine communities, seaweeds must escape, deter, or tolerate herbivory. The ecological and evolutionary importance of spatial and temporal escapes has been extensively studied for seaweeds and adequately reviewed in the recent literature (33, 45, 47, 71, 80). The ability of seaweeds to tolerate herbivory has received limited attention. On coral reefs, rapidly growing filamentous algae are heavily grazed, but the algae quickly replace these losses and appear to be dependent upon herbivores to prevent their habitat from being overgrown by larger but less herbivoretolerant species (11, 71). Additionally, several seaweeds have spores or vegetative portions that can withstand gut passage; in some cases this significantly increases the growth rates of the newly settled spores (6, 122). These types of seaweeds may be considered herbivore tolerant. Although numerous seaweed characteristics can deter some herbivores, the effects of morphology and chemistry have been studied most thoroughly. The
722 citations
"Marine chemical ecology: chemical s..." refers background in this paper
...In aquatic systems, chemical cues determine feeding, habitat, and mating choices (e.g., Hay & Fenical 1988, 1996; Pawlik 1992; Breithaupt & Thiel 2008)....
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...…on the plants they consume and that are especially susceptible to predation suggest that feeding preferences are commonly driven by the need to colonize hosts that provide escapes from consumers rather than by the direct food value of those hosts (see also Hay & Fenical 1988, 1996; Hay 1992, 1996)....
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...In the past 20 years, the review of selected aspects of marine chemical ecology has become a growth industry (e.g., Hay & Fenical 1988, 1996; Paul 1992; Hay 1996; McClintock & Baker 2001; Paul et al. 2007; Pohnert et al. 2007; Amsler 2008), with numerous reviews focusing on specific groups…...
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TL;DR: The contention that furanones, at the concentrations produced by the alga, can control bacterial colonization of surfaces by specifically interfering with AHL-mediated gene expression at the level of the LuxR protein is supported.
Abstract: Summary: Acylated homoserine lactone (AHL)-mediated gene expression controls phenotypes involved in colonization, often specifically of higher organisms, in both marine and terrestrial environments. The marine red alga Delisea pulchra produces halogenated furanones which resemble AHLs structurally and show inhibitory activity at ecologically realistic concentrations in AHL bioassays. Evidence is presented that halogenated furanones displace tritiated OHHL [N-3- (oxohexanoy1)-L-homoserine lactone] from Escherichia coli cells overproducing LuxR with potencies corresponding to their respective inhibitory activities in an AHL-regulated bioluminescence assay, indicating that this is the mechanism by which furanones inhibit AHL-dependent phenotypes. Alternative mechanisms for this phenomenon are also addressed. General metabolic disruption was assessed with two-dimensional PAGE, revealing limited non- AHL-related effects. A direct chemical interaction between the algal compounds and AHLs, as monitored by 1H NMR spectroscopy, was shown not to occur in vitro. These results support the contention that furanones, at the concentrations produced by the alga, can control bacterial colonization of surfaces by specifically interfering with AHL-mediated gene expression at the level of the LuxR protein.
612 citations
"Marine chemical ecology: chemical s..." refers background in this paper
...This inhibition occurs because halogenated furanones interfere with the bacteria’s signal-based regulatory systems that control surface motility, exoenzyme production, and biofilm formation/stability (Manefield et al. 1999, 2002; Rasmussen et al. 2000; McDougald et al. 2001)....
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TL;DR: This review concludes that relatively unstudied, ontogenetic shifts in concentrations and types of defenses occur in marine species, and patterns of larval chemical defenses appear to provide insights into the evolution of complex life cycles and of differing modes of development among marine invertebrates.
607 citations
"Marine chemical ecology: chemical s..." refers background in this paper
...…on the plants they consume and that are especially susceptible to predation suggest that feeding preferences are commonly driven by the need to colonize hosts that provide escapes from consumers rather than by the direct food value of those hosts (see also Hay & Fenical 1988, 1996; Hay 1992, 1996)....
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...In other instances the larvae are chemically defended, but the adults are not and appear instead to rely more on physical/structural defenses (Lindquist & Hay 1996)....
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...…past 20 years, the review of selected aspects of marine chemical ecology has become a growth industry (e.g., Hay & Fenical 1988, 1996; Paul 1992; Hay 1996; McClintock & Baker 2001; Paul et al. 2007; Pohnert et al. 2007; Amsler 2008), with numerous reviews focusing on specific groups (seaweeds…...
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...Once larvae or embryos are released from brooding adults, they can be at considerable risk of predation in the plankton, but even more so as they recruit to the benthos where both fish and invertebrate predators are commonly concentrated (Lindquist & Hay 1996)....
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...…of resistance to host chemical defenses, selective consumption of those hosts, being cued to feed by the specific host chemicals that deter other consumers, and sequestration by the specialist of its host’s chemical defenses, thus becoming immune to many of its own enemies (Hay 1992, 1996)....
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