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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Journal Article•DOI•

Evidence for Strain-Specific Exometabolomic Responses of the Coccolithophore Emiliania huxleyi to Grazing by the Dinoflagellate Oxyrrhis marina

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Kelsey L. Poulson-Ellestad¹, Elizabeth Harvey¹, Matthew D. Johnson¹, Tracy J. Mincer¹•Institutions (1)

Woods Hole Oceanographic Institution¹

28 Jan 2016-Frontiers in Marine Science

TL;DR: High-resolution mass spectrometry is used in an untargeted approach to survey the suite of low molecular weight compounds released by four different E. huxleyi strains in response to grazing by the dinoflagellate Oxyrrhis marina and demonstrates the impact of strain diversity and grazing on the complexity of dissolved organic matter in marine systems.

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Abstract: The coccolithophore Emiliania huxleyi forms massive blooms and plays a critical role in global elemental cycles, sequestering significant amounts of atmospheric carbon dioxide on geological time scales via production of calcium carbonate coccoliths and emitting dimethyl sulfoniopropionate (DMSP) which has the potential for increasing atmospheric albedo. Because grazing in pelagic systems is a major top-down force structuring microbial communities, the influence of grazers on E. huxleyi populations has been of interest to researchers. Roles of DMSP (and related metabolites) in interactions between E. huxleyi and protist grazers have been investigated, however, little is known about the release of other metabolites that may influence, or be influenced by, such grazing interactions. We used high-resolution mass spectrometry in an untargeted approach to survey the suite of low molecular weight compounds released by four different E. huxleyi strains in response to grazing by the dinoflagellate Oxyrrhis marina. Overall, a strikingly small number of metabolites were detected from E. huxleyi and O. marina cells, but these were distinctly informative to construct metabolic footprints. At most, E. huxleyi strains shared 25% of released metabolites. Furthermore, there appeared to be no unified metabolic response in E. huxleyi strains to grazing; rather these responses were strain specific. Concentrations of several metabolites also positively correlated with grazer activities, including grazing, ingestion, and growth rates; however, no single metabolite responded uniformly across all strains of E. huxleyi tested. Regardless, grazing clearly transformed the constituents of dissolved organic matter produced by these marine microbes. This study addresses several technical challenges, and presents a platform to further study the influence of chemical cues in aquatic systems and demonstrates the impact of strain diversity and grazing on the complexity of dissolved organic matter in marine systems.

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6 citations

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

...These waterborne metabolites can be tracked by grazers looking for prey (Hay, 2009) or by algal conspecifics, in which case these released metabolites may act as alarm cues indicating the presence of a grazer (Lurling, 1998; Van Donk et al., 2011)....
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Journal Article•DOI•

Effects of toxicity and zooplankton selectivity on plankton dynamics under seasonal patterns of viruses with time delay

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Saswati Biswas¹, Pankaj Kumar Tiwari², Samares Pal¹•Institutions (2)

Kalyani Government Engineering College¹, Indian Institutes of Information Technology²

14 Sep 2021-Mathematical Methods in The Applied Sciences

6 citations

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

...A1 > 0, A4 > 0, A1A2 − A3 > 0, A3(A1A2 − A3) − A(2)1A4 > 0, (14)...
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...According to Routh-Hurwitz criterion, system (1) is stable at the equilibrium E∗ provided conditions in (14) are satisfied....
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Journal Article•DOI•

An unusual microbiome characterises a spatially-aggressive crustose alga rapidly overgrowing shallow Caribbean reefs.

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Bryan R. Wilson¹, Chen-Ming Fan², Peter J. Edmunds³•Institutions (3)

University of Oxford¹, Carnegie Institution for Science², California State University³

30 Nov 2020-Scientific Reports

TL;DR: The results show that the microbial communities on peyssonnelid algal crusts are characterized by significantly lower numbers of the epibiotic bacterial genus Pseudoalteromonas, which facilitates the recruitment and settlement of marine invertebrates, and infer that PAC are therefore unlikely to be attractive as settlement sites for coral larvae.

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Abstract: Several species of crustose coralline algae (CCA) and their associated microbial biofilms play important roles in determining the settlement location of scleractinian corals on tropical reefs. In recent decades, peyssonnelid algal crusts (PAC) have become spatial dominants across large areas of shallow Caribbean reefs, where they appear to deter the recruitment of scleractinians. Our genetic investigations of PAC in St. John, US Virgin Islands, amplifying the large-subunit ribosomal RNA and psbA protein D1 marker genes, revealed them to be identical to Ramicrusta textilis previously reported overgrowing corals in Jamaica. Specimens of PAC sampled from the Honduras were likewise identical, confirming that this crustose alga inhabits the easternmost and westernmost regions of the Caribbean. We also analysed 16S rDNA tag amplicon libraries of the biofilms associated with PAC and sympatric CCA, which is favoured for coral settlement. Our results show that the microbial communities on PAC (vs. CCA) are characterized by significantly lower numbers of the epibiotic bacterial genus Pseudoalteromonas, which facilitates the recruitment and settlement of marine invertebrates. From these data, we infer that PAC are therefore unlikely to be attractive as settlement sites for coral larvae. Given the significant ecological change anticipated on these reefs due to increasing cover of PAC, there is an urgent need to further investigate competitive interactions between PAC and scleractinian corals, and elucidate the role of PAC and their associated microbiomes in accentuating phase shifts from coral to algae on tropical reefs.

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6 citations

Journal Article•DOI•

Predatory cues drive colony size reduction in marine diatoms.

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Kristie Rigby¹, Erik Selander¹•Institutions (1)

University of Gothenburg¹

14 Jul 2021-Ecology and Evolution

TL;DR: In this article, the authors test the hypothesis that predation is one of the drivers behind colony formation and chain length plasticity in non-motile marine phytoplankton and find that two of the studied species reduce their chain length in response to the presence of copepod grazers.

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Abstract: Colony formation is a common feature among nonmotile marine phytoplankton. Several theories exist around the potential benefits of larger colonies.Here, we test the hypothesis that predation is one of the drivers behind colony formation and chain length plasticity. We exposed cultures of Thalassiosira rotula, Chaetoceros curvisetus, and Chaetoceros affinis to copepodamides, a chemical alarm cue released by copepods and perceived as an indicator of predation threat by their prey. This was coupled with a grazing experiment, which compared copepod grazing rates on different chain lengths.Our results show that T. rotula and C. curvisetus decreased their chain lengths by 79% and 49%, respectively, in response to copepodamides. Single cells and short chains were grazed at lower rates compared with long chains, and the copepodamide-driven size shift led to 30% and 12% lower grazing in T. rotula and C. curvisetus, respectively. In contrast, C. affinis showed a slight increased chain length in response to copepodamides although nonsignificant.We found that 2 of 3 studied species reduce their chain length in response to the presence of copepod grazers. Altered size structure has implications for the route of carbon in the marine food webs and carbon export to deeper strata.

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5 citations

Journal Article•DOI•

Effect of neuroactive compounds on larval metamorphosis of New Zealand geoduck (Panopea zelandica)

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Dung V. Le¹, Tim Young¹, Andrea C. Alfaro¹, Ellie Watts², Nick King² - Show less +1 more•Institutions (2)

Auckland University of Technology¹, Cawthron Institute²

01 Jun 2017-Aquaculture Research

TL;DR: None of the tested chemicals increased the proportion of metamorphosed geoducks, and in some cases, the chemical caused significant mortality, despite having been used extensively with other species, such as mussels and oysters.

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Abstract: We present here the first laboratory study on the effects of pharmacologically active compounds on the larval metamorphosis of the New Zealand geoduck, Panopea zelandica (Quoy and Gaimard, 1835). Two batches of competent hatchery-reared larvae were exposed to acetylcholine chloride, epinephrine hydrochloride and excess potassium ions in the form of KCl and K2SO4. None of the tested chemicals increased the proportion of metamorphosed geoducks, and in some cases, the chemical caused significant mortality, despite having been used extensively with other species, such as mussels and oysters. This might indicate that geoduck larval physiology and development differs from other bivalves. Geoducks may have evolved distinct chemoreceptor patterns that facilitate metamorphosis under environmentally favourable conditions for subtidal soft sediment habitats suitable for burrowing. Thus, further research is needed to identify alternative cues (e.g. conspecific adults, sediment characteristics and surface biofilm) and understand their role in settlement and metamorphosis. This information will aid the design of reseeding methods and contribute to the development of reliable hatchery production of geoduck spat.

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5 citations

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References

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Journal Article•

Chemical ecology of the settlement of benthic marine invertebrates

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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)....
[...]
...…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

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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.

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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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