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•

Investigating the ecology and evolution of cryptic marine nematode species through quantitative real-time PCR of the ribosomal ITS region.

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Sofie Derycke¹, R. Sheibani Tezerji², R. Sheibani Tezerji¹, Annelien Rigaux¹, Tom Moens¹ - Show less +1 more•Institutions (2)

Ghent University¹, Austrian Institute of Technology²

01 Jul 2012-Molecular Ecology Resources

TL;DR: The qPCR assay developed here provides the ability to quickly identify and quantify cryptic nematode species and will facilitate their study in laboratory and field settings.

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Abstract: The presence of morphologically similar but genetically distinct species has impacted biogeographical and ecological paradigms. In marine sediments, free-living nematodes form one of the most abundant and diverse faunal groups. Inferring the importance of nematode diversity for ecosystem functioning requires species-level identification, which is hampered by the lack of easily observable diagnostic characters and the presence of cryptic species. New techniques are urgently needed to adequately study the ecology and evolution of cryptic species. The aim of the present study was to evaluate the potential of a quantitative real-time PCR (qPCR) assay using the internal transcribed spacer (ITS) region of the ribosomal DNA to detect and quantify cryptic species of the R. (P.) marina complex. All primer pairs proved to be highly specific, and each primer pair was able to detect a single juvenile in a pool of 100 nematodes. C(t) values were significantly different between developmental stages for all species except for PmIII. Despite differences between developmental stages, a strong correlation was observed between the amount of extracted DNA and the number of nematodes present. Relative and absolute quantification estimates were comparable and resulted in strong positive correlations between the qPCR estimate and the actual number of nematodes present in the samples. The qPCR assay developed here provides the ability to quickly identify and quantify cryptic nematode species and will facilitate their study in laboratory and field settings.

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25 citations

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

...1998) as well as for ecological interactions (Hay 2009)....
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...This is because most marine species do not require morphological recognition for mating, but instead rely on chemical cues for mate choice and gamete recognition (Stanhope et al. 1992; Palumbi 1994; Lonsdale et al. 1998) as well as for ecological interactions (Hay 2009)....
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Journal Article•DOI•

Effects of adrenoceptor compounds on larval metamorphosis of the mussel Mytilus coruscus

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Jin-Long Yang, Wu-Shuang Li¹, Xiao Liang¹, Yi-Feng Li¹, Yu-Ru Chen¹, Wei-Yang Bao², Jiale Li¹ - Show less +3 more•Institutions (2)

Shanghai Ocean University¹, Yangzhou University²

20 Apr 2014-Aquaculture

TL;DR: These adrenergic agonists can be used as non-toxic and promising inducers of larval metamorphosis in this species, and to improve M. coruscus larval production for aquaculture.

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25 citations

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

...Chemical cues have been known to play an important role in the process of larval settlement and metamorphosis (Hadfield and Paul, 2001; Hay, 2009; Paul et al., 2011; Pawlik, 1992)....
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Journal Article•DOI•

A Review of "Polychaeta" Chemicals and their Possible Ecological Role.

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Marina Cyrino Leal Coutinho¹, Valéria Laneuville Teixeira¹, Cinthya Simone Gomes Santos¹•Institutions (1)

Federal Fluminense University¹

01 Jan 2018-Journal of Chemical Ecology

TL;DR: The present review covers articles published through December 2016 that address marine natural products produced from polychaetes, with a focus on antipredatory strategies, competitors, fouling, and pathogens, and provides a basis for future research on the marine chemical ecology of polychaeta.

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Abstract: Despite the many publications concerning the isolation of substances and the many reviews of marine natural products, some groups of organisms remain poorly studied, including "Polychaeta". In response, this review covers articles published through December 2016 that address marine natural products produced from polychaetes, with a focus on antipredatory strategies, competitors, fouling, and pathogens. A total of 121 compounds were isolated from 1934 to 2016, which includes halogenated aromatics, proteins, amino acids and Lumazine derivatives most notably-with a defensive function were found in the literature, most frequently in the families Sabellidae, Terebellidae, Glyceridae, and Nereididae. The period of highest discovery of natural products in defensive actions for the group was the 2000s. Polychaetes were addressed in 26 revisions of the total 51 articles analyzed and are less reported than other marine invertebrates such as sponges, cnidarians, mollusks, and tunicates. In sum, the present review provides a basis for future research on the marine chemical ecology of polychaetes.

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25 citations

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

...In summary, the ecological importance of natural products has been evaluated experimentally (Hay 1984; Paul and Fenical 1986; Pawlik et al. 1995; McClintock and Baker 1997; Amsler et al. 2005; Hay 2009), and many such natural products, including terpenes, alkaloids, and polyphenols, have been isolated and described for sessile marine organisms, including sponges, ascidians, corals, bryozoans, and algae (Pawlik 1993; Hay and Fenical 1996)....
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...…products has been evaluated experimentally (Hay 1984; Paul and Fenical 1986; Pawlik et al. 1995; McClintock and Baker 1997; Amsler et al. 2005; Hay 2009), and many such natural products, including terpenes, alkaloids, and polyphenols, have been isolated and described for sessile marine…...
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...…habitat and partners, and the behavior of organisms, which affect not only individual or population processes, but also the organization of the community and the functioning of the ecosystem, thereby posing ecological and evolutionary consequences (Hay 1996; Hay and Fenical 1996; Hay 2009, 2011)....
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...…toxin production), intraspecific communication, chemical signaling (e.g., of conspecific danger, for breeding, with pheromones, for attracting prey, and for larval settlement control), protection against ultraviolet radiation, pigmentation, and bioluminescence (Pawlik 1993; Hay 1996, 2009, 2011)....
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Journal Article•DOI•

Predation constrains host choice for a marine mesograzer

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Rachel S. Lasley-Rasher¹, Douglas B. Rasher, Zachary H. Marion, Richard B. Taylor, Mark E. Hay - Show less +1 more•Institutions (1)

Georgia Institute of Technology¹

28 Jul 2011-Marine Ecology Progress Series

TL;DR: It is suggested that seaweed refuge quality, not nutritional quality, drives A. typica host preference and distribution in this system.

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Abstract: For small sedentary herbivores that inhabit seaweeds, choosing a host that provides adequate nutrition and refuge should be favored by natural selection. Yet, the relative importance of seaweed nutritional value versus habitat quality in driving mesograzer host choice remains poorly understood for most herbivores. Previous work in coastal North Carolina, USA, and 2 tropical locations suggests that amphipods often utilize host seaweeds that offer superior refuge from both omni vorous and carnivorous consumers. Our study was conducted in New Zealand, where carnivores alone are the major consumers of seaweed-dwelling amphipods. We show that the herbivorous amphipod Aora typica preferentially utilizes the dictyotalean seaweed Dictyota kunthii over a dominant canopy-forming kelp, Ecklonia radiata, and that this preferred seaweed host provides a superior refuge from predators in both laboratory and field experiments. There was no difference in A. typica feeding preference between D. kunthii and E. radiata, but A. typica grew faster when reared on E. radiata. These results suggest that seaweed refuge quality, not nutritional quality, drives A. typica host preference and distribution in this system.

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25 citations

Journal Article•DOI•

Ocean acidification alters temperature and salinity preferences in larval fish.

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Jennifer C. A. Pistevos¹, Ivan Nagelkerken¹, Tullio Rossi¹, Sean D. Connell¹•Institutions (1)

University of Adelaide¹

01 Feb 2017-Oecologia

TL;DR: This study shows that freshwater species that spend part of their life cycle in the ocean might also be affected by ocean acidification, and that behavioural responses towards key physicochemical cues can also be negated through elevated CO2 from human emissions.

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Abstract: Ocean acidification alters the way in which animals perceive and respond to their world by affecting a variety of senses such as audition, olfaction, vision and pH sensing. Marine species rely on other senses as well, but we know little of how these might be affected by ocean acidification. We tested whether ocean acidification can alter the preference for physicochemical cues used for dispersal between ocean and estuarine environments. We experimentally assessed the behavioural response of a larval fish (Lates calcarifer) to elevated temperature and reduced salinity, including estuarine water of multiple cues for detecting settlement habitat. Larval fish raised under elevated CO2 concentrations were attracted by warmer water, but temperature had no effect on fish raised in contemporary CO2 concentrations. In contrast, contemporary larvae were deterred by lower salinity water, where CO2-treated fish showed no such response. Natural estuarine water-of higher temperature, lower salinity, and containing estuarine olfactory cues-was only preferred by fish treated under forecasted high CO2 conditions. We show for the first time that attraction by larval fish towards physicochemical cues can be altered by ocean acidification. Such alterations to perception and evaluation of environmental cues during the critical process of dispersal can potentially have implications for ensuing recruitment and population replenishment. Our study not only shows that freshwater species that spend part of their life cycle in the ocean might also be affected by ocean acidification, but that behavioural responses towards key physicochemical cues can also be negated through elevated CO2 from human emissions.

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25 citations

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

...The sensory sensitivity (the ability to correctly identify a cue) and relevant responses of an organism to its physicochemical environment are often critical to their survival, and therefore, can also have population-level consequences (Réale et al. 2007; Hay 2009)....
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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)....
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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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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)....
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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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