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•

Stage-specific effects of Lobophora on the recruitment success of a reef-building coral

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Nicolas R. Evensen¹, Christopher Doropoulos², Kelly J. Wong, Peter J. Mumby¹•Institutions (2)

University of Queensland¹, Commonwealth Scientific and Industrial Research Organisation²

16 Apr 2019-Coral Reefs

TL;DR: The results indicate that Lobophora most heavily impacts coral recruitment by inhibiting larval settlement, with the impact of the alga on recruitment decreasing through later life-history stages.

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Abstract: Benthic marine organisms rely on the dispersal and recruitment of propagules to replenish depleted populations following disturbances. Yet, ecological interactions between colonizing larvae and benthic competitors that become established following a disturbance can be a primary driver of recruitment success. On some coral reefs, local and global stressors have led to a proliferation of macroalgae that can inhibit the recruitment and recovery of corals. The brown macroalga Lobophora is considered a particularly strong inhibitor of coral recruitment, yet there is little information on how the alga affects demographic bottlenecks across early life-history stages. In the present study, we conducted a series of experiments to determine the effects of Lobophora sp. on three distinct life-history stages of the coral Acropora digitifera: larval settlement, early post-settlement survival, and survival and growth of small nubbins (1 cm) created from adult colonies. Our results demonstrate a high sensitivity of coral larvae to Lobophora, with settlement decreasing 16-fold when the alga was present on tiles compared to controls. Moreover, larvae did not settle on tiles when Lobophora cover > 50%. A negative, albeit minor, effect of Lobophora on the early post-settlement survival was evident, despite few recorded incidents of direct competition between settled corals and Lobophora because of low larval settlement in proximity to the alga. Conversely, there was no effect of Lobophora on the growth and survival of coral nubbins. Our results indicate that Lobophora most heavily impacts coral recruitment by inhibiting larval settlement, with the impact of the alga on recruitment decreasing through later life-history stages. These findings are concurrent with recent studies that demonstrate the ability of particular macroalgal species to deter coral larvae from settling on degraded reefs, likely through the release of chemical compounds, thereby impacting the recovery of coral populations following disturbances.

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16 citations

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

...Once competent to settle, larvae rely on a mixture of environmental cues to locate appropriate microhabitats (Rodriguez et al. 1993; Hadfield and Paul 2001; Hay 2009), a process influenced by the availability of settlement space and nature of cues present (Roughgarden et al. 1985; Hay 2009)....
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Journal Article•DOI•

Effects of newt chemical cues on the distribution and foraging behavior of stream macroinvertebrates

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Gary M. Bucciarelli¹, Lee B. Kats²•Institutions (2)

University of California, Los Angeles¹, Pepperdine University²

01 May 2015-Hydrobiologia

TL;DR: The hypothesis that chemical stimuli from predators, and TTX specifically, can shape species interactions at lower trophic levels and potentially affect community organization is supported.

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Abstract: Many amphibians possess noxious or toxic substances for self defense. These compounds have been characterized largely as chemical defenses, but may promote ecological and evolutionary processes. The California newt, Taricha torosa, possesses a potent neurotoxin, tetrodotoxin (TTX), which serves as a chemical defense, chemical cue to conspecifics, and selection pressure that has selected for evolved resistance in a predator. However, the potential effects of TTX upon the broader community and on behavior, in general, have been overlooked. Field assays conducted during the newt breeding season indicate that the macroinvertebrate community responds to adult newt chemical cues by altering foraging behavior. In these assays, significantly fewer macroinvertebrates were found in experimental areas with enclosed newts relative to enclosures with a non-predatory amphibian. Laboratory bioassays showed that dragonfly nymphs (Anax junius) reduced predatory behavior and moved less in the presence of adult newt chemical cues. When exposed to TTX, nymph mean angular velocities were reduced four fold and mean velocity magnitude was reduced threefold relative to controls. Overall, these results support the hypothesis that chemical stimuli from predators, and TTX specifically, can shape species interactions at lower trophic levels and potentially affect community organization.

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16 citations

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

...…as well as other organisms within the community (Petranka et al., 1987; Dahl, 1998; Turner et al., 2000; Hay & Kubanek, 2002; Pohnert et al., 2007; Hay, 2009), and facilitate numerous ecological processes (Pawlik, 1992; Hadfield & Paul, 2001; Roberts & Uetz, 2005; Chivers et al., 1996; Tamburri…...
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...…can affect community organization, trophic webs, and biogeochemical processes has been proposed (McClintock & Baker, 2001; Pohnert et al., 2007; Hay, 2009), and in marine systems these effects can reverberate throughout ecosystems, ultimately affecting structure and function (Hay & Kubanek,…...
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Journal Article•DOI•

A Stable-Isotope Mass Spectrometry-Based Metabolic Footprinting Approach to Analyze Exudates from Phytoplankton

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Ralf J. M. Weber¹, Erik Selander, Ulf Sommer¹, Mark R. Viant¹•Institutions (1)

University of Birmingham¹

29 Oct 2013-Marine Drugs

TL;DR: An algorithm was developed to automatically pinpoint just those metabolites with highly 13C-enriched isotope signatures, allowing us to discover algal exudates from the complex seawater background, and will facilitate the discovery of novel dissolved bioactive compounds.

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Abstract: Phytoplankton exudates play an important role in pelagic ecology and biogeochemical cycles of elements. Exuded compounds fuel the microbial food web and often encompass bioactive secondary metabolites like sex pheromones, allelochemicals, antibiotics, or feeding attractants that mediate biological interactions. Despite this importance, little is known about the bioactive compounds present in phytoplankton exudates. We report a stable-isotope metabolic footprinting method to characterise exudates from aquatic autotrophs. Exudates from 13C-enriched alga were concentrated by solid phase extraction and analysed by high-resolution Fourier transform ion cyclotron resonance mass spectrometry. We used the harmful algal bloom forming dinoflagellate Alexandrium tamarense to prove the method. An algorithm was developed to automatically pinpoint just those metabolites with highly 13C-enriched isotope signatures, allowing us to discover algal exudates from the complex seawater background. The stable-isotope pattern (SIP) of the detected metabolites then allowed for more accurate assignment to an empirical formula, a critical first step in their identification. This automated workflow provides an effective way to explore the chemical nature of the solutes exuded from phytoplankton cells and will facilitate the discovery of novel dissolved bioactive compounds.

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16 citations

Book Chapter•DOI•

Identification of Crustacean Sex Pheromones

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Joerg D. Hardege¹, John A. Terschak•Institutions (1)

University of Hull¹

01 Jan 2010

TL;DR: The principles of a bioassay-driven purification that is combined with a metabolomic approach where differences in the odor profiles of sexually active and inactive crabs are examined are described and the female produced signal is identified to be a nucleotide with its production being linked with the female molt (ecdysis).

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Abstract: Odor and fragrances can carry information about an organism and have long been suggested as vital mechanisms that affect or control animal behavior. The use of such chemical signals is widespread in the aquatic environment, and crustaceans such as lobsters, shrimps, crabs, barnacles, and crayfish are known to utilize odor for predator–prey interactions, mating, establishing of dominance or social hierarchies as well as hatching of young and settlement of larvae. Nevertheless, the chemical identity of these behavior-modifying odors remains largely unknown. Here, we briefly review the literature on crustacean chemical signals and describe our approach to identify these using the example of the shore crab (Carcinus maenas) sex pheromones. We describe the principles of a bioassay-driven purification that is combined with a metabolomic approach where differences in the odor profiles of sexually active and inactive crabs are examined. Using such an integrated approach, we identified the female produced signal to be a nucleotide with its production being linked with the female molt (ecdysis). The pheromone enables males to detect the optimal time to mate just after the female molt with the timing of the reproductive event enabling crabs to use a simple, not species-specific, chemical as a sex pheromone. Based on our recent findings, we discuss the implications for future studies on crustacean chemical signaling.

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15 citations

Journal Article•DOI•

Using insights from animal behaviour and behavioural ecology to inform marine conservation initiatives

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Rohan M. Brooker¹, William E. Feeney¹, William E. Feeney², William E. Feeney³, James R. White⁴, R. P. Manassa⁵, Jacob L. Johansen⁶, Danielle L. Dixson¹ - Show less +4 more•Institutions (6)

University of Delaware¹, University of Queensland², University of Cambridge³, James Cook University⁴, Monash University⁵, Marine Science Institute⁶

01 Oct 2016-Animal Behaviour

TL;DR: Whether incorporation of knowledge from the fields of animal behaviour and behavioural ecology may improve the effectiveness of conservation initiatives in marine systems is investigated and understanding the behavioural and physiological responses of species to a changing environment is considered.

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15 citations

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References

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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)]....
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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)....
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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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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)....
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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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