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

Abstract

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.

Nitrogenous compounds characterized in the deterrent skin extract of migratory adult sea lamprey from the Great Lakes region

“…Given the Agnatha is ancestral to all gnathostomes, and the lack of conservation of alarm cue chemistry at larger phylogenetic distances as evidenced by a lack of response to heterospecific cues from distant vs. close relatives [33,75,76]. The sea lamprey also exhibits declining behavioral response to alarm cues collected from confamilial species of Petromyzontide, but fail to respond to cues from more ancestral (Atlantic hagfish, Myxine glutinosa, Myxinidae, Agnatha) and derived (white sucker, Catastomus commersonii , Catastomidae, Actinopterygii) taxa [40]. Further, the process of Soxhlet extraction at high temperature (70–80°C) for multiple hours does not degrade the reactivity of the extract vs. that derived from grinding and freezing skin [13, Wagner et al, in review].…”

“…In the relatively well-studied Ostariophysan fishes, evidence has accrued to suggest these alarm substances include a variety of water soluble nitrogenous compounds including amino acids and oligopeptides [29,30], hypoxanthine-3-N-oxide and similar compounds containing the nitrogen-oxide functional group of purine-N-oxides [31–33], histamine [34], protein, possibly as a carrier molecule [35], and glycosaminoglycan chondroitin [36]. Further, mixtures of odorants are expected to compose each alarm cue, as full behavioral reactivity appears species specific, with partial overlap observed among related species [37,38] including lampreys [39,40].…”

A Neuro-Inspired Computational Model for a Visually Guided Robotic Lamprey Using Frame and Event Based Cameras

“…Lamprey and other organisms have been found to be capable of adapting their behaviors based on danger cues sensed in their surrounding environments [27]. Damage-released alarm cues originating from conspecific organisms under distress mark regions as high-risk, and can instigate the animals' alarm responses [28]. Experiments have even shown that certain fish species are able to learn from such odor cues, which are believed to play a role in teaching organisms to recognize new entities as predators.…”

Attenuation and recovery of an avoidance response to a chemical antipredator cue in an invasive fish: implications for use as a repellent in conservation

“…Fish alarm cues, substances released from damaged tissue that elicit antipredator behaviour in conspecifics (= schreckstoff per von Frisch, 1938 , 1941 ), have been extensively studied (for recent reviews, see Ferrari et al , 2010 ; Wisenden, 2015 ). Alarm cues are suspected to be mixtures of compounds, as cross-reactivity is limited to confamilial species, and behavioural responses tend to diminish with increasing phylogenetic distance between the emitter and receiver species ( Hazlett and McLay, 2005 ; Dalesman et al , 2007 ; Schoeppner and Relyea, 2009 ; Mitchell et al , 2012 ; Hume and Wagner, 2018 ). The compounds that compose the mixture are principally detected by ciliated olfactory sensory neurons (OSNs) that stimulate the medial olfactory tract, inducing avoidance or other antipredator responses ( Hamdani and Døving, 2002 , 2007 ; Døving and Lastein, 2009 ).…”