Field verification of chondroitin sulfate as a putative component of chemical alarm cue in wild populations of fathead minnows (Pimephales promelas)

Faulkner, Alexai; Holstrom, Ingrid E.; Molitor, Samantha A.; Hanson, Mikaela E; Shegrud, Whitney R.; Gillen, Joshua C.; Willard, Samuel J.; Wisenden, Brian D.

doi:10.1007/s00049-017-0247-z

Cited by 12 publications

(10 citation statements)

References 28 publications

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“…Therefore, the function of these compounds as alarm cues likely evolved secondarily as an honest signal of predation when presented alongside additional chemical compounds (e.g., the odor or predators themselves), producing a chemical mixture that cannot be manipulated to the benefit of predator over prey (Bradbury & Vehrencamp, 2000;Guilford & Dawkins, 1991). Among fishes, chemical compounds functioning as alarm cues may have evolved primarily as antimicrobial and UV protective compounds and contained in epidermal cells (Chivers, Wisenden, et al, 2007;Chivers, Zhao, et al, 2007;Faulkner et al, 2017;Halbgewachs, Marchant, Kusch, & Chivers, 2009). Damage to the epidermis of these fish during an attack would release these chemicals into the environment and become available to receivers.…”

Section: Discussionmentioning

confidence: 99%

“…The most parsimonious view of the evolution of this phenomenon is that alarm cues initially evolved to provide separate fitness‐enhancing functions (e.g., immunity, Chivers, Wisenden et al., ; Chivers, Zhao, & Ferrari, ) and had no association with predation events specifically. However, during an attack, these and other chemical compounds may be perceived together as a mixture that is capable of providing both an indication of predation and the identity of the species involved (Faulkner et al., ; Wisenden, ). Presumably, over evolutionary time, gradual changes to these chemical compounds responsible for initiating antipredator behaviors result in only partial recognition of the cue, regardless of whether both species continue to overlap spatially and share predators.…”

Section: Introductionmentioning

confidence: 99%

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A death in the family: Sea lamprey (Petromyzon marinus) avoidance of confamilial alarm cues diminishes with phylogenetic distance

Hume

Wagner

2018

Ecology and Evolution

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Alarm signals released after predator attack function as reliable public information revealing areas of high risk. The utility of this information can extend beyond species boundaries, benefiting heterospecifics capable of recognizing and responding appropriately to the signal. Nonmutually exclusive hypotheses explaining the acquisition of heterospecific reactivity to cues suggest it could be conserved phylogenetically following its evolution in a common ancestor (a species‐level effect) and/or learned during periods of shared risk (a population‐level effect; e.g., shared predators). Using a laboratory‐based space‐use behavioral assay, we tested the response of sea lamprey (Petromyzon marinus) to the damage‐released alarm cues of five confamilial (sympatric and allopatric) species and two distantly related out‐groups: a sympatric teleost (white sucker Catostomus commersonii) and an allopatric agnathan (Atlantic hagfish Myxine glutinosa). We found that sea lamprey differed in their response to conspecific and heterospecific odors; exhibiting progressively weaker avoidance of cues derived from more phylogenetically distant confamilials regardless of current overlap in distribution. Odors from out‐groups elicited no response. These findings suggest that a damage‐released alarm cue is at least partially conserved within the Petromyzontidae and that sea lamprey perceives predator attacks directed to closely related taxa. These findings are consistent with similar observations from gastropod, amphibian and bony fish taxa, and we discuss this in an eco‐evo context to provide a plausible explanation for the acquisition and maintenance of the response in sea lamprey.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A death in the family: Sea lamprey (Petromyzon marinus) avoidance of confamilial alarm cues diminishes with phylogenetic distance

Hume

Wagner

2018

Ecology and Evolution

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“…Active compounds in skin extract probably include hypoxanthine 3(N) oxide (Brown et al 2000(Brown et al , 2001(Brown et al , 2003Parra et al, 2009), but empirical support for hypoxanthine 3(N) oxide as the sole active ingredient has not survived careful scrutiny (Ferrari et al, 2010;Mathuru et al, 2012;Wisenden, 2015). There is biochemical evidence that chondroitin sulphate is a component of alarm cue in Danio rerio (Mathuru et al, 2012), northern studfish Fundulus catenatus (Storer 1846) (Farnsley et al, 2016) and P. promelas (Faulkner et al, 2017), but, similar to hypoxanthine 3(N) oxide, chondroitin sulphate does not confer full potency relative to raw-skin extract and also lacks species specificity. Alarm cue is most likely to be a mixture of compounds that confer some phylogenetically inherited components and other components that are species-specific (Wisenden, 2015).…”

Section: Discussionmentioning

confidence: 99%

Olfactorily‐mediated cortisol response to chemical alarm cues in zebrafish Danio rerio

Barkhymer

Garrett

Wisenden

2018

Journal of Fish Biology

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Chemical cues released as a by‐product of predation mediate antipredator behaviour, but little is known about the physiological responses to olfactory detection of predation risk. In this study, zebrafish Danio rerio were exposed to either chemical alarm cues from conspecifics, or water (control). Compared with water controls, D. rerio exposed to alarm cues responded behaviourally with antipredator behaviours such as erratic dashing and an increase in time spent near the bottom of the test aquarium. Danio rerio were sacrificed 5 min after exposure to test cues (alarm cues or water). Enzyme‐linked immunosorbent assay (ELISA) revealed whole‐body levels of cortisol that were significantly higher for fish exposed to alarm cues (mean ± SE, 11.9 ± 3.4 ng g−1) than control fish (1.5 ± 0.7 ng g−1). These data provide a benchmark for future studies of the proximate mechanisms of olfactorily mediated antipredator responses, modelling effects on aquatic life in a changing climate and, as a model organism, Danio rerio can further our understanding of anxiety in humans.

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“…This led to the suggestion that the nitrogen oxide functional group is important in initiating antipredator behavior, but is anchored to purine rings that differ in structure across taxa, allowing for species specificity in the cue (Brown et al 2003). Another compound, chondroitin sulfate, elicits alarm responses in zebrafish (Mathuru et al 2012) and fathead minnows (Faulkner et al 2017), but the activity is less than the cue produced by injured tissue from the same species, suggesting the alarm cue is a mixture. One common pattern that has arisen is the response to alarm cues obtained from closely related taxa, where the magnitude of the alarm response declines with increasing phylogenetic distance between the cue donor and the responding species (Mirza and Chivers 2001;Mitchell, Cowman, & Mccormick, 2012;Schoeppner and Relyea 2009;Mathis and Smith 1993).…”

Section: Introductionmentioning

confidence: 99%

Sea Lamprey Alarm Cue Comprises Water- and Chloroform- Soluble Components

et al. 2022

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A diversity of aquatic organisms manage predation risk by avoiding waters activated with conspecific alarm cues, a chemical mixture released from injuries. The sea lamprey (Petromyzon marinus) is a nocturnal migratory species that relies on its alarm cue to navigate around areas of predation risk when moving through river channels. Identification of the cue’s chemistry would allow managers to harness this innate behavioral response to guide migrating sea lamprey to traps (invasive population in the Laurentian Great Lakes) or to fish passage devices where dams block migrations in their native range. We pursued isolation of the sea lamprey alarm cue through behaviorally guided fractionation, fractionating the alarm cue into water-soluble and chloroform-soluble fractions, each of which elicited a substantial avoidance response. Recombining the two fractions restored full reactivity, suggesting the alarm cue mixture contains components that exhibit high solubility in water (e.g., nitrogenous compounds), chloroform (e.g., lipids), or perhaps materials that dissolve readily in either solvent. We further screened 13 individual compounds or pure isolates and 6 sub-fractions from the water-soluble fraction and found one of the pure isolates, isoleucine, evoked an avoidance response on its own, but not consistently when found in other mixtures. In a third experiment, we observed no behavioral response after recombining 32 compounds isolated and identified from the water-soluble fraction. These results confirm other suggestions that the process of elucidating alarm cue constituents is challenging. However, we suggest the pursuit is worthwhile given the strong evidence for the utility of alarm cues for use in the conservation and management of fishes and other aquatic organisms.

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Field verification of chondroitin sulfate as a putative component of chemical alarm cue in wild populations of fathead minnows (Pimephales promelas)

Cited by 12 publications

References 28 publications

A death in the family: Sea lamprey (Petromyzon marinus) avoidance of confamilial alarm cues diminishes with phylogenetic distance

A death in the family: Sea lamprey (Petromyzon marinus) avoidance of confamilial alarm cues diminishes with phylogenetic distance

Olfactorily‐mediated cortisol response to chemical alarm cues in zebrafish Danio rerio

Sea Lamprey Alarm Cue Comprises Water- and Chloroform- Soluble Components

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