Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems.

doi:10.1146/ANNUREV.MARINE.010908.163708

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Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems.

Journal Article•DOI•

Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems.

Mark E. Hay¹•Institutions (1)

Georgia Institute of Technology¹

25 Mar 2009-Annual Review of Marine Science (Annual Reviews)-Vol. 1, Iss: 1, pp 193-212

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.

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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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Book Chapter•DOI•

A Review of the Ecological Role of Chemical Defenses in Facilitating Biological Invasion by Marine Benthic Organisms

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Bruno G. Lages¹, Beatriz G. Fleury¹, Joel C. Creed¹•Institutions (1)

Rio de Janeiro State University¹

01 Jan 2015-Studies in natural products chemistry

TL;DR: A number of examples where chemical compounds might be the key of invasion success are presented but, conclusions are still hindered in drawing clear conclusions regarding the relative importance of these chemical traits by a lack of knowledge of the chemical ecology of most marine organisms.

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Abstract: The marine biological invasion of nonindigenous species (NIS) into new areas is a growing conservation concern for marine ecologists around the world. NIS may bring loss of diversity and extinctions of endemic organisms as well as trigger changes in the function and structure of marine ecosystems, often with profound economic consequences. This review considers the role of the chemical ecology of NIS in the process of marine biological invasion. NIS oftentimes use their arsenal of chemical substances, acquired in their previous evolutionary context, to surmount obstacles presented by novel predators and competitors to success in the new invaded habitat. Alternatively, the escape from energetically costly chemical production at origin may allow more efficient establishment and expansion of NIS into new areas. We present a number of examples where chemical compounds might be the key of invasion success but, we are still hindered in drawing clear conclusions regarding the relative importance of these chemical traits by a lack of knowledge of the chemical ecology of most marine organisms.

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9 citations

Journal Article•DOI•

Cell density-dependent swimming patterns of Alexandrium fundyense early stationary phase cells

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Agneta Persson, Barry C. Smith

18 Mar 2013-Aquatic Microbial Ecology

TL;DR: It is suggested that chemical attraction between gametes causes the observed behavior of early stationary phase A. fundyense cells, both on the individual level and on the population level.

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Abstract: Different life-history stages of Alexandrium fundyense have different swimming behaviors and show different responses to water movement. Early stationary phase cells assemble in bioconvection patterns along the water surface and as stripes in the water, while cells in exponential growth do not. We studied the swimming behavior of early stationary phase A. fundyense cells, both on the individual level and on the population level. Cells assembled in spots in shallow Petri dishes, and were studied using an inverted microscope. We analyzed 53 videos of cells at different distances from the center of accumulated spots of cells with the program CellTrak for swimming behavior of individual cells. The closer the cells were to the center of spots, the faster they swam (>600 μm s−1 in the center of spots compared to ca. 300 μm s−1 outside) and the more often they changed direction (>1400 degrees s−1 in the center compared to <400 degrees s−1 outside). On a population level, the behavior of spots of assembled cells was studied using time-lapse photo graphy. The spots entrained more and more cells as they grew and fused with each other; the closer the spots came to each other, the faster they moved until they fused. We suggest that chemical attraction between gametes causes the observed behavior.

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9 citations

Journal Article•DOI•

Effects of plant growth regulators on physiological performances of three calcifying green macroalgae Halimeda species (Bryopsidales, Chlorophyta)

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Zhangliang Wei¹, Chao Long¹, Fangfang Yang¹, Lijuan Long¹, Jiahao Mo¹, Qunju Hu¹, Yuanzi Huo², Dewen Ding¹, Dewen Ding³ - Show less +5 more•Institutions (3)

Chinese Academy of Sciences¹, University of Maryland Center for Environmental Science², Ontario Ministry of Natural Resources³

01 Feb 2020-Aquatic Botany

TL;DR: It is both practical and efficient to amplify calcifying Halimeda biomass through the addition of PGRs, which could provide a theoretical basis for use of this technique in restoring and maintaining the ecological diversity and sustainable development of coral reef ecosystems.

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9 citations

Journal Article•DOI•

Adding early-stage engineering species affects advanced-stage organization of shallow-water fouling assemblages

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Edson A. Vieira¹, Edson A. Vieira², Gustavo Muniz Dias¹, Augusto A. V. Flores³•Institutions (3)

Universidade Federal do ABC¹, State University of Campinas², University of São Paulo³

17 Apr 2018-Hydrobiologia

TL;DR: The hypotheses that richness and community structure are positively affected by founder-richness at more advanced stages are tested, and that such effect may depend on the functional traits of founders (more or less prone to facilitate other species).

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Abstract: Although commonly overlooked, processes determining early patterns of species assembly may affect community dynamics and diversity at advanced states. In this study, we followed richness and community structure in experimental units pioneered by single or multiple species, within a given functional group—colonial ascidians, arborescent, and encrusting bryozoans. We tested the hypotheses that richness and community structure are positively affected by founder-richness at more advanced stages, and that such effect may depend on the functional traits of founders (more or less prone to facilitate other species). More diverse founding assemblages of arborescent bryozoans led to richer communities after 1 and 5 months of succession, with no effects observed for the other functional groups. Assemblages started by a single species were dominated by space monopolizers (encrusting bryozoans), while the ones founded by two species were characterized by a higher abundance of engineering forms (arborescent bryozoans), which may provide a physically complex substrate suitable to both the attraction and protection of other species recruits. Both effects on advanced-stage richness and community structure reflect the importance of facilitation through founder diversity and functionality in community organization.

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9 citations

Cites background from "Marine chemical ecology: chemical s..."

...Facilitation through increased settlement rates may well be mediated through positive chemical interactions in which larvae are attracted by bacterial biofilms that cover bryozoan branches (Dahms et al., 2004; Hay, 2009)....
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Journal Article•

Water-borne cues induce chemical defense in a marine alga (Ascophyllum nodosum). [Erratum: Apr 10, 2001, v. 98 (8), p. 4815.]

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G.B. Toth, H. Pavia

01 Jan 2000-Proceedings of the National Academy of Sciences of the United States of America

TL;DR: In this article, the authors show that water-borne cues from actively feeding herbivorous gastropods, flat periwinkles (Littorina obtusata), can serve as external signals to induce production of defense chemicals (phlorotannins) in unharmed individuals of seaweeds, knotted wrack (Ascophyllum nodosum), and that the increased levels of defence chemicals deter further feeding by periwinks.

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Abstract: It is well known that herbivores can induce chemical defenses in terrestrial vascular plants, but few examples of inducible production of defense chemicals have been reported for aquatic macrophytes. Furthermore, it is well established that water-borne chemical cues from predators or predator-wounded conspecifics can induce defensive changes of aquatic prey animals, but no such communication between aquatic herbivores and seaweeds has been reported. Here we show that water-borne cues from actively feeding herbivorous gastropods, flat periwinkles (Littorina obtusata), can serve as external signals to induce production of defense chemicals (phlorotannins) in unharmed individuals of seaweeds, knotted wrack (Ascophyllum nodosum), and that the increased levels of defense chemicals deter further feeding by periwinkles. Because seaweeds have poorly developed internal-transport systems and may not be able to elicit systemic-induced chemical defenses through conveyance of internal signals, this mechanism ensures that seaweeds can anticipate future periwinkle attacks without receiving direct damage by herbivores.

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8 citations

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References

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Open Access

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Journal Article•

Chemical ecology of the settlement of benthic marine invertebrates

[...]

Joseph R. Pawlik

01 Jan 1992-Oceanography and Marine Biology

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)....
[...]
...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)]....
[...]

Journal Article•DOI•

Centuries of Human-Driven Change in Salt Marsh Ecosystems

[...]

K. Bromberg Gedan¹, Brian R. Silliman¹, Mark D. Bertness²•Institutions (2)

Brown University¹, University of Florida²

25 Mar 2009-Annual Review of Marine Science

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.

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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.

...read moreread less

770 citations

Journal Article•DOI•

Marine Plant-Herbivore Interactions: The Ecology of Chemical Defense

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Mark E. Hay, William Fenical

01 Jan 1988-Annual Review of Ecology, Evolution, and Systematics

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.

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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

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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)....
[...]
...…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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Journal Article•DOI•

Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein.

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Mike Manefield¹, Rocky de Nys¹, Kumar Naresh¹, Read Roger¹, Michael Givskov², Steinberg Peter¹, Staffan Kjelleberg¹ - Show less +3 more•Institutions (2)

University of New South Wales¹, Technical University of Denmark²

01 Feb 1999-Microbiology

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.

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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.

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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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Journal Article•DOI•

Marine chemical ecology: what's known and what's next?

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Mark E. Hay¹•Institutions (1)

University of North Carolina at Chapel Hill¹

15 Nov 1996-Journal of Experimental Marine Biology and Ecology

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.

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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)....
[...]
...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)....
[...]
...…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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