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

doi:10.1146/ANNUREV.MARINE.010908.163708

Home
/
Papers
/
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.

read less

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...

...read moreread less

Content maybe subject to copyright Report

Citations

PDF

Open Access

More filters

Journal Article•DOI•

Impacts of Global Warming and Elevated CO2 on Sensory Behavior in Predator-Prey Interactions: A Review and Synthesis

[...]

Alex M. Draper¹, Marc J. Weissburg¹•Institutions (1)

Georgia Institute of Technology¹

01 Mar 2019-Frontiers in Ecology and Evolution

TL;DR: A framework for understanding how warming and elevated CO2 can alter behavioral interactions is developed by examining how the processes (steps) of sensory cue production, transmission and reception may change, and it is suggested that some modalities may be particularly prone to disruption.

...read moreread less

Abstract: Ecosystems are shaped by complex interactions between species and their environment. However, humans are rapidly changing the environment through increased carbon dioxide (CO2) emissions, creating global warming and elevated CO2 levels that affect ecological communities through multiple processes. Understanding community responses to climate change requires examining the consequences of changing behavioral interactions between species, such as those affecting predator and prey. Understanding the underlying sensory process that govern these interactions, and how they may be affected by climate change provides a predictive framework, but many studies examine behavioral outcomes only. This review summarizes the current knowledge of global warming and elevated CO2 impacts on predator-prey interactions with respect to the relevant aspects of sensory ecology, and we discuss the potential consequences of these effects. Our specific questions concern how climate change affects the ability of predators and prey to collect information and how this affects predator-prey interactions. We develop a framework for understanding how warming and elevated CO2 can alter behavioral interactions by examining how the processes (steps) of sensory cue (or signal) production, transmission and reception may change. This includes both direct effects on cue production and reception resulting from changes in organismal physiology, but also effects on cue transmission resulting from modulation of the physical environment via physical and biotic changes. We suggest that some modalities may be particularly prone to disruption, and that aquatic environments may suffer more serious disruptions as a result of elevated CO2 and warming that collectively affect all steps of the signaling process. Temperature by itself may primarily operate on aspects of cue generation and transmission, implying that sensory-mediated disruptions in terrestrial environments may be less severe. However, significant biases in the literature in terms of modalities (chemosensation), taxa (fish), and stressors (elevated CO2) examined currently prevents accurate generalizations. Significant issues such as multimodal compensation and altered transmission or other environmental effects remain largely unaddressed. Future studies should strive to fill these knowledge gaps in order to better understand and predict shifts in predator-prey interactions in a changing climate.

...read moreread less

60 citations

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

...It could be that detection of specific predator cues were affected whereas food cues were not, as they are typically composed of a number of different molecules (Hay, 2009)....
[...]
...These chemical classes are important in attracting predators to prey (Hay, 2009) and also may be important constituents of risk cues released by predators (Poulin et al....
[...]
...These chemical classes are important in attracting predators to prey (Hay, 2009) and also may be important constituents of risk cues released by predators (Poulin et al., 2018)....
[...]

Journal Article•DOI•

A review of predator diet effects on prey defensive responses

[...]

Avery E. Scherer¹, Delbert L. Smee¹•Institutions (1)

Texas A&M University–Corpus Christi¹

05 Mar 2016-Chemoecology

TL;DR: The value of responding based on a predator’s recent diet increased when predators specialized more strongly on particular prey species, which may create patterns in diet cue use among prey depending upon whether they are preyed upon by generalist or specialist predators.

...read moreread less

Abstract: Numerous studies have examined how predator diets influence prey responses to predation risk, but the role predator diet plays in modulating prey responses remains equivocal. We reviewed 405 predator–prey studies in 109 published articles that investigated changes in prey responses when predators consumed different prey items. In 54 % of reviewed studies, prey responses were influenced by predator diet. The value of responding based on a predator’s recent diet increased when predators specialized more strongly on particular prey species, which may create patterns in diet cue use among prey depending upon whether they are preyed upon by generalist or specialist predators. Further, prey can alleviate costs or accrue greater benefits using diet cues as secondary sources of information to fine tune responses to predators and to learn novel risk cues from exotic predators or alarm cues from sympatric prey species. However, the ability to draw broad conclusions regarding use of predator diet cues by prey was limited by a lack of research identifying molecular structures of the chemicals that mediate these interactions. Conclusions are also limited by a narrow research focus. Seventy percent of reviewed studies were performed in freshwater systems, with a limited range of model predator–prey systems, and 98 % of reviewed studies were performed in laboratory settings. Besides identifying the molecules prey use to detect predators, future studies should strive to manipulate different aspects of prey responses to predator diet across a broader range of predator–prey species, particularly in marine and terrestrial systems, and to expand studies into the field.

...read moreread less

59 citations

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

...Some prey alter their morphology to make it more difficult for predators to eat them (Schoeppner and Relyea 2005) or manufacture higher levels of chemical defenses to deter potential consumers (Baldwin 1998; Hay 2009)....
[...]
...Chemical cues are commonly used to gather information regarding predation risk by many taxa ranging from microbes to vertebrates (Hay 2009), even among organisms that rely heavily on other sensory modalities such as vision (Weissburg et al. 2014)....
[...]
...Chemical cues are commonly used to gather information regarding predation risk by many taxa ranging from microbes to vertebrates (Hay 2009), even among organisms that rely heavily on other sensory modalities such as vision (Weissburg et al....
[...]

Journal Article•DOI•

The Neuroecology of Dimethyl Sulfide: A Global-Climate Regulator Turned Marine Infochemical

[...]

Gabrielle A. Nevitt¹•Institutions (1)

University of California, Davis¹

01 Nov 2011-Integrative and Comparative Biology

TL;DR: Using a neuroecological approach, this work has established that these biogenic sulfur compounds serve as critical signal molecules in marine systems and provides a more mechanistic understanding of how climate change may impact information transfer within marine food webs.

...read moreread less

Abstract: Information transfer influences food-web dynamics in the marine environment, but infochemicals involved in these processes are only beginning to be understood. Dimethylsulfoniopropionate (DMSP) is produced by phytoplankton and other marine algae, and has been studied primarily in the context of sulfur cycling and regulation of global climate. My laboratory has been investigating DMSP and its breakdown product, dimethyl sulfide as infochemicals associated with trophic interactions in marine habitats, including sub-Antarctic and coral reef ecosystems. Using a neuroecological approach, our work has established that these biogenic sulfur compounds serve as critical signal molecules in marine systems and provides us with a more mechanistic understanding of how climate change may impact information transfer within marine food webs.

...read moreread less

57 citations

Journal Article•DOI•

Seaweed allelopathy against coral: surface distribution of a seaweed secondary metabolite by imaging mass spectrometry.

[...]

Tiffany D. Andras¹, Troy S. Alexander¹, Asiri Gahlena¹, R. Mitchell Parry¹, Facundo M. Fernández¹, Julia Kubanek¹, May D. Wang¹, Mark E. Hay¹ - Show less +4 more•Institutions (1)

Georgia Institute of Technology¹

30 Oct 2012-Journal of Chemical Ecology

TL;DR: It is shown that contact with four common seaweeds induces bleaching on natural colonies of Porites rus, and for allelopathy of lipid-soluble metabolites to be effective, the compounds would need to be deployed on algal surfaces where they could transfer to corals on contact.

...read moreread less

Abstract: Coral reefs are in global decline, with seaweeds increasing as corals decrease. Although seaweeds inhibit coral growth, recruitment, and survivorship, the mechanism of these interactions is poorly understood. Here, we used field experiments to show that contact with four common seaweeds induces bleaching on natural colonies of Porites rus. Controls in contact with inert, plastic mimics of seaweeds did not bleach, suggesting seaweed effects resulted from allelopathy rather than shading, abrasion, or physical contact. Bioassay-guided fractionation of the hydrophobic extract from the red alga Phacelocarpus neurymenioides revealed a previously characterized antibacterial metabolite, neurymenolide A, as the main allelopathic agent. For allelopathy of lipid-soluble metabolites to be effective, the compounds would need to be deployed on algal surfaces where they could transfer to corals on contact. We used desorption electrospray ionization mass spectrometry (DESI-MS) to visualize and quantify neurymenolide A on the surface of P. neurymenioides, and we found the molecule on all surfaces analyzed, with highest concentrations on basal portions of blades.

...read moreread less

57 citations

Journal Article•DOI•

Competition induces allelopathy but suppresses growth and anti-herbivore defence in a chemically rich seaweed

[...]

Douglas B. Rasher¹, Mark E. Hay¹•Institutions (1)

Georgia Institute of Technology¹

22 Feb 2014-Proceedings of The Royal Society B: Biological Sciences

TL;DR: The first demonstration of induced allelopathy in a seaweed, or of competitors reducing seaweed chemical defences against herbivores, is demonstrated, suggesting that the chemical ecology of coral–seaweed–herbivore interactions can be complex and nuanced.

...read moreread less

Abstract: Many seaweeds and terrestrial plants induce chemical defences in response to herbivory, but whether they induce chemical defences against competitors (allelopathy) remains poorly understood. We evaluated whether two tropical seaweeds induce allelopathy in response to competition with a reef-building coral. We also assessed the effects of competition on seaweed growth and seaweed chemical defence against herbivores. Following 8 days of competition with the coral Porites cylindrica, the chemically rich seaweed Galaxaura filamentosa induced increased allelochemicals and became nearly twice as damaging to the coral. However, it also experienced significantly reduced growth and increased palatability to herbivores (because of reduced chemical defences). Under the same conditions, the seaweed Sargassum polycystum did not induce allelopathy and did not experience a change in growth or palatability. This is the first demonstration of induced allelopathy in a seaweed, or of competitors reducing seaweed chemical defences against herbivores. Our results suggest that the chemical ecology of coral–seaweed–herbivore interactions can be complex and nuanced, highlighting the need to incorporate greater ecological complexity into the study of chemical defence.

...read moreread less

57 citations

1
2
3
4
5
6
7
8
…
9
10
11
12
13
14
15
…
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73
74
75
76
77
78
79
80
81
82
83
84
85
86
87

Collapse

References

PDF

Open Access

More filters

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)....
[...]
...…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.

...read moreread less

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

[...]

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.

...read moreread less

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

...read moreread less

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)....
[...]
...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…...
[...]

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.

[...]

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.

...read moreread less

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.

...read moreread less

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)....
[...]

Journal Article•DOI•

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

[...]

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.

...read moreread less

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