No Need to be Alarmed

Authors: Olivia Davis, Lauren Spangler and Phil McNamara

Biology Department, University of Washington, Seattle, WA 98195

Pheromones are chemical substances that serve especially as social stimuli to other individuals of the same species for one or more behavioral responses (Karlson & Luscher, 1959).  While it was once thought that only eukaryotes were able to use chemical cell signaling, it was found to also occur in bacteria (Miller & Bassler, 2003). Studies have shown that species ranging from bacteria to humans (Radulescu & Mujica-Parodi, 2013) can use chemical signals in a variety of ways, including as a sexual attractant (Katona, 1973), for establishing territory (Traniello, 1989), as well as for chemical alarm cues (Meuthen, Baldauf, &Thünken, 2015). How do different species use pheromones and how do other members of the species respond effectively?

One way many species have been able to use pheromones to their advantage is through alarm cues. In the presence of a predator, a chemical alarm cue can be produced by the sender (the prey), effectively warning others, particularly members of the same species, of the present danger. However, the sender of the signal may not survive (Meuthen, Baldauf, & Thünken, 2015). What is the evolutionary benefit? How did chemical alarm cues evolve? One popular scientific hypothesis for this advantage is the kin selection hypothesis. The kin selection hypothesis states that by sending an alarm cue to kin, kin will respond, ensuring the sender’s genetic material will be passed on to future offspring, even if the sender does not survive. For example, Richard Karban and colleagues found that plant’s kin respond more effectively to chemical signals than non-kin (Karban, Shiojiri, Ishizaki, Wetzel, & Evans, 2013). Additionally, Eastern chipmunks send out alarm calls in the presence of a predator to increase their inclusive fitness by potentially saving their kin from such predators(Burke da Silva, Mahan, & da Silva, 2002).  Denis Meuthen, Sebastian A Baldauf, and Timo Thünken attempt to shed further light on this topic by using the cichlid fish species Pelvicachromis taeniatus, to test the effects of kin alarm cues vs non-kin alarm cues on the behavior of these fish (Meuthen et al., 2015).

Alarm cues are not just found in P. taeniatus, but throughout many species of fish.  Many coral fish species use chemical alarm cues in the presence of predators (Mitchell, Cowman, & McCormick, 2012) as do rainbow trout, which may be important in teaching hatchery fish to recognize chemical alarm cues (Brown & Smith, 2011). The common link between most alarm signals in fish seems to be that the chemical alarm cue is transmitted when the fish is injured. Minnows have been shown to have a chemical in their skin cells that is released when the cells become damaged (Wisenden, Vollbrecht, & Brown, 2004). What has yet to be completely understood, however, is why such a mechanism evolved. Some studies have reported that releasing chemical alarm cues has a direct benefit to the sender. For example, in a study by Doug P. Chivers and colleagues, they suggested that the alarm cells in the skin of fishes may be able to protect the fish against pathogens, parasites, and UVB radiation after injury (Chivers et al., 2007). Yet the kin selection hypothesis has remained a possibility as well.

To explore further, do fish respond better to alarm cues from relatives?  Discovering the answer to this question may help further our understanding of why chemical alarm cues evolved, as it seems that the sender of a chemical alarm cue has low chance of survival and may receive little direct benefit in emitting any sort of signal at all. Additionally, alarm cues are expensive to produce, which brings even more question to their possible fitness benefit. How did a mechanism with so little benefit to the sender of the alarm cue develop and evolve over time? Understanding what an individual could gain from emitting chemical alarm signals is vital to understanding the evolution of chemical signaling. In their study, Meuthen and colleagues offer further insight into this puzzling question.

davis--olivia_3164215_30477316_Figure Evo Devo Draft 2 copy

The nature of alarm signals provided a problem for evolutionary biologists. Upon predation, certain fish phylogenies release a chemical substance into the water called “schreckstoff,” which serves as an alarm signal for other nearby prey (Irving and Magurran, 1997). Chemical signals released into the water disperse broadly and it is impossible for only the relatives of the deceased to get a benefit. Thus when it comes to intra-species competition, producing schreckstoff appears to provide no advantage. In 2012, Denis Meuthen and his research team looked at a possible solution to this problem: that fish can sense the signals of their kin and respond to them in a way that non-kin cannot. This would give a greater survival rate to relatives of the dying fish in a predatory attack and increase its fitness.

In order to assess the hypothesis that fish respond better to the signals of their kin, Meuthen and his colleagues experimented on P. taeniatus, a cichlid known to respond to chemical alarm signals. Schreckstoff was generated by euthanizing cichlids and grinding them with a mortar and pestle, simulating a lethal predation event. Female cichlids were then exposed to normal water, water containing an alarm signal from a related fish, or water containing a signal from an unrelated fish. Their movement was monitored using a video camera, as the response by cichlids to a potential predator is to remain still. Although movement decreased in the presence of the schreckstoff, no significant difference was observed in the response to kin vs. non-kin signals (p = 0.63).  Fish were also measured for standard length and weighed for body mass, which did not differ between the three treatments. From these results the authors concluded that cichlids cannot distinguish kin from non-kin signals and that the kin selection hypothesis does not fully explain the evolution of schreckstoff.

The fact that cichlids cannot differentiate between alarm signals does not rule out the role of kin selection, but it does necessitate alternative hypotheses. One such idea was developed by Douglas P. Chivers et al., who found that schreckstoff production was not stimulated by increased predation but instead by skin parasites and UV radiation. The idea of evolutionary traits taking on a secondary function is known as exaptation and is well established. Feathers most likely evolved as an efficient form of heat regulation before their use in flight (Barve and Wagner, 2013). The function of schreckstoff as an alarm signal could have evolved later, with its fitness value coming from its immune function. Another idea is that because P. taeniatus have behaviors of kin-shoaling (Hesse and Thünken, 2014), kin selection could still be at work because the receivers that get the benefit from the alarm cue are kin of the sender. Since these fish live in kin groups, this means that most of the time the fish that sends an alarm cue will be sending the cue to kin, and therefore increases the inclusive fitness of the sender.

Kin selection theory has been upheld by several experiments across many different species. However, Meuthen and colleagues’ (2012) experiment contrasts these previous findings in that they found that P. taeniatus did not have different responses between kin and non-kin alarm cues. However, the alarm cues from kin and non-kin alike did decrease the activity of prey which would increase their survival in the presence of visual predators. The authors explained that their results show no direct or indirect link between alarm cues and kin cues, but this does not mean kin were not recognized in the fish since kin could have been recognized during trials. The authors argued that because of the behaviour of P. taeniatus such as kin-shoaling (Hesse and Thünken, 2014) and their ability to identify and live in kin-shaped groups (Ward and Hart, 2003), kin discrimination in alarm cues did not have to evolve in P. taeniatus . Since P. taeniatus already lives and mostly associates with kin it wasn’t needed for alarm cues to have a stronger response from kin because kin were already receiving benefit from alarm cues due to their close association with each other. So, as the author suggest kin selection theory may still be at work here but through more indirect means then other experiments have shown.

Future questions that should be considered for this topic would be if P. taeniatus schreckstoff is possibly an exaptation, what were the evolutionary mechanisms to drive schreckstoff as an alarm cue? Another question related to the previous one would be: what are the direct benefits of schreckstoff as an immune enhancing mechanism? Also, could the evolution of kin-shoaling and other behaviours of P. taeniatus be an indirect form of kin selection when alarm cues are dispersed? Further research should be concluded to answer these questions and to determine the direct costs and benefits to senders and receivers of alarm cues. However, Meuthen and colleagues (2012) presented a new way to look at the kin selection theory, which is that the direct mechanisms may not be present but indirect factors can play a role in ensuring kin survivability and thus indirectly increasing the sender’s fitness. Further, they demonstrated that evolution is complex and that all the mechanisms of it are still not completely known. The broader implications of these findings is that other species of vertebrates, plants, and invertebrates that use alarm signals and pheromones to communicate to other members of it’s species may be using these chemical signals for more than one purpose. It might be possible for species that form tight living groups with kin and regularly use pheromones and chemical signaling to communicate with each other, that they may as well be using their alarm signals when a predator is near as an indirect form of kin selection, similar to Meuthen and colleagues experiment (2012). This would mean that the research into chemical signaling between species and how these signals evolved needs to be further examined with the thought of indirect kin selection in mind. As Kocher and Grozinger (2011) described, “Elucidation of the factors that led to the evolution of complex chemical communication systems is challenging: it requires characterization of both proximate and ultimate factors underlying pheromone production and response” (p. 1271). Chemical signaling is highly complex and great care and consideration must be taken into researching how these mechanisms evolved not only in P. taeniatus but in the countless number of organisms that use pheromones and chemical signaling.

REFERENCES

Chivers, Douglas P et al. “Epidermal ‘Alarm Substance’ Cells of Fishes Maintained by Non-Alarm Functions: Possible Defence against Pathogens, Parasites and UVB Radiation.” Proceedings. Biological sciences / The Royal Society 274.August (2007): 2611–2619. Web.

Mitchell, Matthew D, Peter F Cowman, and Mark I McCormick. “Chemical Alarm Cues Are Conserved within the Coral Reef Fish Family Pomacentridae.” PloS one 7.10 (2012): e47428. Web. 5 Feb. 2015.

Radulescu, Anca R, and Lilianne R Mujica-Parodi. “Human Gender Differences in the Perception of Conspecific Alarm Chemosensory Cues.” PloS one 8.7 (2013): e68485. Web. 6 Feb. 2015.

Zulandt Schneider, R a, and P a Moore. “Urine as a Source of Conspecific Disturbance Signals in the Crayfish Procambarus Clarkii.” The Journal of experimental biology 203 (2000): 765–771. Print.

Burke da Silva K, Mahan C, da Silva J. “The Trill of the Chase: Eastern Chipmunks Call to Warn Kin.” J Mammal. (2002): 546–552. Web.

Karban R, Shiojiri K, Ishizaki S, Wetzel WC, Evans RY. “Kin Recognition Affects Plant Communication and Defence.” Proc R Soc / Biol Sci. (2013): 280. Web. 6 Feb. 2015.

Hesse S, Thünken T. “Growth and Social Behavior in a Cichlid Fish are Affected by Social Rearing Environment and Kinship.” Naturwissenschaften. (2014): 273–283.Web.

Ward AJW, Hart PJB. “The Effects of Kin and Familiarity on Interactions Between Fish.” Fish Fish. (2003): 348–358. Web. 6 Feb. 2015.

Kocher SD, Grozinger CM. “Cooperation, Conflict, and the Evolution of Queen Pheromones.”      J Chem Ecol. (2011): 1263-1275. Web. 13 Feb. 2015.

Meuthen, D., Baldauf, S. A., & Thünken, T. (2015). Evolution of alarm cues : a test of the kin selection hypothesis, (0). doi:10.12688/f1000research.1-27.v1

Miller, M. B., & Bassler, B. L. (2003). QUORUM SENSING IN BACTERIA. Retrieved from http://www.annualreviews.org/doi/full/10.1146/annurev.micro.55.1.165?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub%3dpubmed&

Wisenden, B. D., Vollbrecht, K. a., & Brown, J. L. (2004). Is there a fish alarm cue? Affirming evidence from a wild study. Animal Behaviour, 67(Smith 1992), 59–67. doi:10.1016/j.anbehav.2003.02.010

Brown, G. E., & Smith, R. J. F. (2011). Acquired predator recognition in juvenile rainbow trout (Oncorhynchus mykiss): conditioning hatchery-reared fish to recognize chemical cues of a predator. Canadian Journal of Fisheries and Aquatic Sciences.

Irving, P. “Context-dependent Fright Reactions in Captive European Minnows: The Importance of Naturalness in Laboratory Experiments.”Animal Behaviour 53.6 (1997): 1193-201.

Barve, Aditya, and Andreas Wagner. “A latent capacity for evolutionary innovation through exaptation in metabolic systems.” National Center for Biotechnology Information. U.S. National Library of Medicine, 6 Aug. 2012.

KARLSON, P., & LUSCHER, M. (1959). Pheromones’: a new term for a class of biologically active substances. Nature, 183(4653), 55–6. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/13622694

KATONA, S. K. (1973). Evidence for sex pheromones in planktonic copepods. Limnology and                                          Oceanography, 18(4), 574–583. doi:10.4319/lo.1973.18.4.0574

Traniello, J. F. A. (1989). Chemical trail systems, orientation, and territorial interactions in the antLasius neoniger. Journal of Insect Behavior, 2(3), 339–354. doi:10.1007/BF01068060

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One thought on “No Need to be Alarmed

  1. Dear Mrs. Davis, Mrs. Spangler and Mr. McNamara,

    I have enjoyed reading your review of my paper. You have succinctly summarized all the important aspects and were able to present them to your readers in a way which is easy to understand.

    For your next review, however, I would suggest you work in a team rather than as individual entities. In some places your review appears as if you have divided the workload into three parts and did not communicate with each other about the respective parts.
    This is why your citation style is very incoherent (in the beginning of the paper you quote it twice as Meuthen, Baldauf & Thünken 2015 (full authors in a three-author papers should be given only at first notion), afterwards as Meuthen et al. 2015. Thereafter you use Meuthen and colleagues (2012) and in the citation list you refer to it as Meuthen et al. (2015). Meuthen et al. 2012 would have been the correct notion as the paper was first published in 2012. You should refer to papers always by the year it was published instead of the year you read it in.
    Another example is that you repeat each other when it comes to explain the relevant theories, for example compare the contents of the paragraph which starts with “Another idea is that[…]” with the paragraph starting off as “The authors explained that […]”.
    A third example would be that you wrote the species name P. taeniatus in italic font (which is the correct way) during the first and last third of the review whereas in the second third species names are written in standard font.
    To avoid these issues in the future, I would suggest you first paste these single segments into a single document. Afterwards, you should take turns in reading through the full paper and correcting or commenting on incoherencies you notice by the comment/correction function which is part of a lot of software options such as for example Microsoft Word and afterwards change the manuscript accordingly.

    Regarding the content I have only minor comments.
    When listing possible benefits of alarm cues, I would have liked to see you include the one theory which considers direct benefits for the sender of alarm cues. It is hypothesized that the release of alarm cues during a predation event may attract secondary predators which engage the first predator, allowing the prey a chance to escape (see “Chivers, D. P., Brown, G. E. & Smith, R. J. F. 1996. The evolution of chemical alarm signals: Attracting predators benefits alarm signal senders. American Naturalist, 148, 649-659.” and Mathis, A., Chivers, D. P. & Smith, R. J. F. 1995. Chemical alarm signals – Predator deterrents or predator attractants. American Naturalist, 145, 994-1005.”).
    Second, you have written “but this does not mean kin were not recognized in the fish since kin could have been recognized during trials.”. Here I would have liked to see a discussion why generally a difference in recognition does not always equal a different response in animals.
    Third, you have mentioned “would increase their survival in the presence of visual predators.” Detection of movement is however not only possible by visual channels. Many fish, including predators, have developed “lateral lines” which are capable of highly sensitive mechanoreception (thus being able to detect water movement induced by prey locomotion). Therefore, reduced movement is not only a viable strategy against visual predators but also against predators which detect prey via mechanoreception.

    Moreover, I have noticed incoherencies in your references section.
    First, you should use standard names or standard abbreviations for specific journals throughout the references section. For example you refer to the same journal once as “Proceedings. Biological sciences / The Royal Society” and later as “Proc R Soc / Biol Sci.”
    Second, titles of papers should be written in lowercase letters except the first letter of the first word (the problem here is that no standard citation format for papers exists when pulling them from online sources which is due to the different citation formats of different scientific journals).
    Third, you should not include notions such as “Web.” or “Print.” in your references list as first many journals are available both online and in print and second other journals are online-only. Instead you should add the volume number of the respective references which is asked for throughout journals.
    Fourth, in some cases you wrote author’s names or paper’s titles in only uppercase letters which is not appropriate.
    Fifth, you referred to author’s names quite differently. Compare for example “Wisenden, B. D., Vollbrecht, K. a., & Brown, J. L.” with “Barve, Aditya, and Andreas Wagner”. You should select one style of how to abbreviate author’s names and stick with it throughout the reference section.

    Lastly, scientific papers should always attempt to further current knowledge; therefore I would have liked to see either an attempt to criticize the applied methods in my paper with a proposition of alternative methods to test the same question. Alternatively, on the basis of my paper you could have presented new hypotheses as starting points for future research including methods as how to test these hypotheses.

    Despite these points which could improve your manuscript, it was a fun read for me and I hope you enjoyed writing your review all the same. Do not worry about the amount of things I pointed out in your work as this is standard procedure throughout scientific research – when working on scientific papers together with colleagues as well as when reviewing papers for journals. The points I listed are not aimed at you personally but rather are intended to improve your future work.

    I wish you best of luck in your future scientific endeavors and if you have any questions about my paper specifically or writing scientific manuscripts in general, feel free to contact me.

    Best wishes,
    Denis

    Dipl. Biol. Denis Meuthen
    University of Bonn
    Institute of Evolutionary Biology and Ecology
    An der Immenburg 1
    53121 Bonn – Germany

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