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The Ancient Chemistry of Avoiding Risks of Predation and Disease

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Abstract

Illness, death, and costs of immunity and injury strongly select for avoidance of predators or contagion. Ants, cockroaches, and collembola recognize their dead using unsaturated fatty acids (e.g., oleic or linoleic acid) as “necromone” cues. Ants, bees, and termites remove dead from their nests (necrophoric behavior) whereas semi-social species seal off corpses or simply avoid their dead or injured (necrophobic behavior). Alarm and avoidance responses to exudates from injured conspecifics are widespread. This involves diverse pheromones, complex chemistry and learning. We hypothesized that necromones are a phylogenetically ancient class of related signals and predicted that terrestrial Isopoda (that strongly aggregate and lack known dispersants) would avoid body fluids and corpses using fatty acid “necromones.” Isopods were repelled by crushed conspecifics (blood), intact corpses, and alcohol extracts of bodies. As predicted, the repellent fraction contained oleic and linoleic acids and authentic standards repelled several isopod species. We further predicted a priori that social caterpillars (lacking known dispersants) would be repelled by their own body fluids and unsaturated fatty acids. Both tent caterpillars and fall webworms avoided branches treated with conspecific body fluid. Oleic and linoleic acids were also strongly avoided by both species. Necromone signaling appears widespread and likely traces to aquatic ancestors pre-dating the divergence of the Crustacea and Hexapoda at least 420 million years ago.

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References

  • Abbott, K. R. (2006). Bumblebees avoid flowers containing evidence of past predation events. Canadian Journal of Zoology, 84, 1240–1247.

    Article  Google Scholar 

  • Akino, T., & Yamaoka, R. (1996). Origin of oleic acid corpse recognition signal in the ant, Formica japonica Motschlsky (Hymenoptera: Formicidae). Japanese Journal of Applied Entomology and Zoology, 40, 265–271.

    CAS  Google Scholar 

  • Almeida, O. G., Miranda, A., Frade, P., Hubbard, P. C., Barata, E. N., & Canario, A. V. M. (2005). Urine as a social signal in the Mozambique tilapia (Oreochromis mossambicus). Chemical Senses, 30(Suppl 1), i309–i310.

    Article  PubMed  Google Scholar 

  • Andersson, K. G., Bronmark, C., Herrmann, J., Malmqvist, B., Otto, C., & Sjorstrom, P. (1986). Presence of sculpins (Cottus gobio) reduces drift and activity of Gammarus pulex (Amphipoda). Hydrobiologia, 133, 209–215.

    Article  Google Scholar 

  • Andre, F., Chaput, N., Schartz, N. E. C., Flament, C., Aubert, N., Bernard, J., et al. (2004). Exosomes as potent cell-free peptide-based vaccine. I. Dendritic cell-derived exosomes transfer functional MHC Class I/peptide complexes to dendritic cells. Journal of Immunology, 172, 2126–2136.

    CAS  Google Scholar 

  • Aqistapace, P., Calamai, L., Hazlett, B. A., & Gherardi, F. (2005). Source of alarm substances in crayfish and their preliminary chemical characterization. Canadian Journal of Zoology, 83, 1624–1630.

    Article  Google Scholar 

  • Arneson, K. O., & Roberts, L. J. (2007). Measurement of products of docosahexaenoic acid peroxidation, neuroprostanes, and neurofurans. Methods in Enzymology, 433, 127–143.

    Article  PubMed  CAS  Google Scholar 

  • Ayasse, M., & Paxton, R. (2002). Brood protection in social insects. In M. Hilker & T. Meiners (Eds.), Chemoecology of insect eggs and egg deposition (pp. 117–148). Berlin: Blackwell.

    Google Scholar 

  • Behringer, D. C., Butler, M. J., & Shields, J. D. (2006). Avoidance of disease by social lobsters. Nature, 441, 421.

    Article  PubMed  CAS  Google Scholar 

  • Beklioglu, M., Telli, M., & Gozen, A. G. (2006). Fish and mucus-dwelling bacteria interact to produce a kairomone that induces diel vertical migration in Daphnia. Freshwater Biology, 51, 2200–2206.

    Article  Google Scholar 

  • Breed, M. D. (1998). Recognition pheromones of the honey bee. BioScience, 48, 470–483.

    Google Scholar 

  • Briones-Fourzan, P., Perez-Ortiz, M., & Lozano-Alvarez, E. (2006). Defense mechanisms and antipredator behavior in two sympatric species of spiny lobsters, Panulirus argus and P. guttatus. Marine Biology, 149, 227–239.

    Article  Google Scholar 

  • Briones-Fourzan, P., Ramirez-Zaldivar, E., & Lozano-Alvarez, E. (2008). Influence of conspecific and heterospecific aggregation cues and alarm odors on shelter choice by syntopic spiny lobsters. Biological Bulletin, 215, 182–190.

    Article  PubMed  Google Scholar 

  • Buchwald, R., & Breed, M. D. (2005). Nestmate recognition cues in a stingless bee, Trigona fulviventris. Animal Behaviour, 70, 1331–1337.

    Article  Google Scholar 

  • Chaput, N., Schartz, N. E. C., Andre, F., Taieb, J., Novault, S., Bonnaventure, P., et al. (2004). Exosomes as potent cell-free peptide-based vaccine. II. Exosomes in CpG adjuvants efficiently prime naive Tc1 lymphocytes leading to tumor rejection. Journal of Immunology, 172, 2137–2146.

    CAS  Google Scholar 

  • Cremer, S., & Sixt, M. (2009). Analogies in the evolution of individual and social immunity. Philosophical Transactions of the Royal Society of London. Series B, 364, 129–142.

    Article  PubMed  Google Scholar 

  • Crosland, M. W. J., & Traniello, J. F. A. (1997). Behavioral plasticity in division of labor in the lower termite Reticulitermes fukienensis. Naturwissenschaften, 84, 208–211.

    Article  CAS  Google Scholar 

  • Davis, J. L. D., Young-Williams, A. C., Aguilar, R., Carswell, B. L., Goodison, M. R., Hines, A. H., et al. (2004). Differences between hatchery-raised and wild blue crabs: Implications for stock enhancement potential. Transactions of the American Fisheries Society, 133, 1–14.

    Article  Google Scholar 

  • Dukas, R. (1998). Ecological relevance of associative learning in fruit fly larvae. Behavioral Ecology and Sociobiology, 45, 195–200.

    Article  Google Scholar 

  • Dukas, R. (2001). Effects of perceived danger on flower choice by bees. Ecological Letters, 4, 327–333.

    Article  Google Scholar 

  • Fadok, V. A., Xue, D., & Henson, P. (2001). If phosphatidylserine is the death knell, a new phosphatidylserine-specific receptor is the bellringer. Cell Death and Differentiation, 8, 582–587.

    Article  PubMed  CAS  Google Scholar 

  • Ferner, M. C., Smee, D. L., & Chang, Y. P. (2005). Cannibalistic crabs respond to the scent of injured conspecifics: Danger or dinner? Marine Ecology Progress Series, 300, 193–200.

    Article  Google Scholar 

  • Fitzgerald, T. D. (1995). The tent caterpillars (p. 303). Ithica, NY: Cornell University Press.

    Google Scholar 

  • Fitzgerald, T. D. (2009). Use of pheromone mimic to cause the disintegration and collapse of colonies of tent caterpillars (Malacosoma spp.). Journal of Applied Entomology, 132, 451–460.

    Article  Google Scholar 

  • Fitzgerald, T. D., & Peterson, S. C. (1988). Cooperative foraging and communication in caterpillars. BioScience, 38, 20–25.

    Article  Google Scholar 

  • Forward, R. B., Jr., & Rittschof, D. (1993). Activation of photoresponses of brine shrimp nauplii involved in diel vertical migration by chemical cues from fish. Journal of Plankton Research, 15, 693–701.

    Article  Google Scholar 

  • Gaunt, M. W., & Miles, M. A. (2002). An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Molecular Biology and Evolution, 19, 748–761.

    PubMed  CAS  Google Scholar 

  • Gelperin, A. (2008). Neural computations with mammalian infochemicals. Journal of Chemical Ecology, 34, 928–942. doi: 10.1007/s10886-008-9483-6.

    Article  PubMed  CAS  Google Scholar 

  • Gordon, D. M. (1983). Dependence of necrophoric response to oleic acid on social context in the ant, Pogonomyrmex badius. Oecologia, 9, 105–111.

    CAS  Google Scholar 

  • Greenberg, M. E., Sun, M., Zhang, R., Febbraio, M., Silverstein, R., & Hazen, S. L. (2006). Oxidized phosphatidylserine-CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells. The Journal of Experimental Medicine, 203, 2613–2625.

    Article  PubMed  CAS  Google Scholar 

  • Hamilton, W. D., & Zuk, M. (1982). Heritable true fitness and bright birds: A role for parasites. Science, 218, 384–387.

    Article  PubMed  CAS  Google Scholar 

  • Hazlett, B. A. (1994). Alarm responses in the crayfish Orconectes virilis and Orconectes propinquus. Journal of Chemical Ecology, 20, 1525–1535.

    Article  Google Scholar 

  • Hazlett, B. A. (2003). The effects of starvation on crayfish responses to alarm odor. Ethology, 109, 587–592.

    Article  Google Scholar 

  • Hazlett, B. A., & McLay, C. (2005). Responses of the crab Heterozius rotundifrons to heterospecific chemical alarm cues: Phylogeny vs. ecological overlap. Journal of Chemical Ecology, 31, 671–677.

    Article  PubMed  CAS  Google Scholar 

  • Holomuzki, J. R., & Hatchett, L. A. (1994). Predator avoidance costs and habituation to fish chemicals by a stream isopod. Freshwater Biology, 32, 585–592.

    Article  Google Scholar 

  • Horner, A. J., Nickles, S. P., Weissburg, M. J., & Derby, C. D. (2006). Source and specificity of chemical cues mediating shelter preference of Caribbean spiny lobsters (Panulirus argus). Biological Bulletin, 211, 128–139.

    Article  PubMed  Google Scholar 

  • Howard, D. F., & Tschinkel, W. R. (1976). Aspects of necrophoric behavior in the red imported fire ant, Solenopsis invicta. Behaviour, 56, 157–178.

    Article  Google Scholar 

  • Hughes, L., Westoby, M., & Jurado, B. (1994). Convergence of elaisomes and insect prey: Evidence from ant foraging behaviour and fatty acid composition. Functional Ecology, 8, 358–365.

    Article  Google Scholar 

  • Hwang, Y. S., Schultz, J. W., & Mulla, M. S. (1984). Structure-activity relationship of unsaturated fatty acids as mosquito ovipositional repellents. Journal of Chemical Ecology, 10, 145–151.

    Article  CAS  Google Scholar 

  • Janzen, D. H. (1977). Why fruits rot, seeds mold, and meat spoils. American Naturalist, 111, 691–713.

    Article  CAS  Google Scholar 

  • Julian, G. E., & Cahan, S. (1999). Undertaking specialization in the desert leaf-cutter ant Acromyrmex versicolor. Animal Behaviour, 58, 437–442.

    Article  PubMed  Google Scholar 

  • Kavaliers, M., Choleris, E., Agmo, A., Braun, W. A., Colwell, D. D., Muglia, L. J., et al. (2006). Inadvertent social information and the avoidance of parasitized male mice: A role for oxytocin. Proceedings of the National Academy of Sciences of the United States of America, 103, 4293–4298.

    Article  PubMed  CAS  Google Scholar 

  • Keller, S., Rupp, C., Stoeck, A., Runz, S., Fogel, M., Lugert, S., et al. (2007). CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney International, 72, 1095–1102.

    Article  PubMed  CAS  Google Scholar 

  • Knepper, M. A., & Pisitkun, T. (2007). Exosomes in urine: Who would have thought…? Kidney International, 72, 1043–1045.

    Article  PubMed  CAS  Google Scholar 

  • Krishna, K., & Grimaldi, D. A. (2003). The first cretaceous Rhinotermitidae (Isoptera): A new species, genus, and subfamily in Burmese amber. American Museum Novitates, 3390, 1–10.

    Article  Google Scholar 

  • Kuenen, D. J., & Nooteboom, H. P. (1963). Olfactory orientation in some land-isopods (Oniscoidea, Crustacea). Entomologia Experimentalis et Applicata, 6, 133–142.

    Article  Google Scholar 

  • Laforsch, C., Beccara, L., & Tollrian, R. (2006). Inducible defenses: The relevance of chemical alarm cues in Daphnia. Limnol. Oceanography, 51, 1466–1472.

    Google Scholar 

  • Lanyon, C. V., Rushton, S. P., O’Donnell, A. G., Goodfellow, M., Ward, A. C., Petrie, M., et al. (2007). Murine scent mark microbial communities are genetically determined. FEMS Microbiology Ecology, 59, 576–583.

    Article  PubMed  CAS  Google Scholar 

  • Lively, C. M., Hazel, W. N., Schellenberger, M. J., & Michelson, K. S. (2000). Predator-induced defense: Variation for inducibility in an intertidal barnacle. Ecology, 81, 1240–1247.

    Google Scholar 

  • Lopez-Riquelme, G. O., Malo, E. A., Cruz-Lopez, L., & Fanjul-Moles, M. L. (2006). Antennal olfactory sensitivity in response to task-related odours of three castes of the ant Atta mexicana (hymenoptera: formicidae). Physiological Entomology, 31, 353–360.

    Article  CAS  Google Scholar 

  • Martin, C., Provost, E., Bagneres, A. G., Roux, M., Clement, J. L., & Le Conte, Y. (2002). Potential mechanism for detection by Apis mellifera of the parasitic mite Varroa destructor inside sealed brood cells. Physiological Entomology, 27, 175–188.

    Article  CAS  Google Scholar 

  • Masterman, R., Ross, R., Mesce, K., & Spivak, M. (2001). Olfactory and behavioral response thresholds to odors of diseased brood differ between hygienic and non-hygienic honey bees (Apis mellifera L.). Journal of Comparative Physiology A, 187, 441–452.

    Article  CAS  Google Scholar 

  • Matsumura, K., Matsunaga, S., & Fusetani, N. (2004). Possible involvement of phosphatidylcholine in school recognition in the catfish, Plotosus lineatus. Zoological Science, 21, 257–264.

    Article  PubMed  CAS  Google Scholar 

  • McKelvey, L. M., & Forward, R. B., Jr. (1995). Activation of brine shrimp nauplii photoresponses involved in diel vertical migration by chemical cues from visual and non-visual planktivores. Journal of Plankton Research, 17, 2191–2206.

    Article  Google Scholar 

  • McKillup, S. C., & McKillup, R. V. (1992). Inhibition of feeding in response to crushed conspecifics by the pebble crab Philyra laevis (Bell). Journal of Experimental Marine Biology and Ecology, 161, 33–43.

    Article  Google Scholar 

  • Moore, A., Ives, M. J., & Kell, L. T. (1994). The role of urine in sibling recognition in Atlantic salmon Salmo salar (L.) parr. Proceedings of the Royal Society B, 255, 173–180.

    Article  Google Scholar 

  • Mothersill, C., Smith, R. W., Agnihotri, N., & Seymour, C. B. (2007). Characterization of a radiation-induced stress response communicated in vivo between zebrafish. Environmental Science and Technology, 41, 3382–3387.

    Article  PubMed  CAS  Google Scholar 

  • Nga, B. T., Lurling, M., Peeters, E., Roijackers, R., Scheffer, M., & Nghia, T. T. (2006). Effects of crushed conspecifics on growth and survival of Penaeus monodon Fabricius post larvae. Aquaculture Research, 37, 224–232.

    Article  Google Scholar 

  • Nichols, Z., & Vogt, R. G. (2008). The SNMP/CD36 gene family in Diptera, Hymenoptera and Coleoptera: Drosophila melanogaster, D. pseudoobscura, Anopheles gambiae, Aedes aegypti, Apis mellifera, and Tribolium castaneum. Insect Biochemistry and Molecular Biology, 38, 398–415.

    Article  PubMed  CAS  Google Scholar 

  • Nijholt, W. W. (1980). Pine oil and oleic acid delay and reduce attacks on logs by ambrosia beetles (Coleoptera: Scolytidae). The Canadian Entomologist, 112, 199–204.

    Google Scholar 

  • Nilsson, E., & Bengtsson, G. (2004a). Endogenous free fatty acids repel and attract Collembola. Journal of Chemical Ecology, 30, 1431–1443.

    Article  PubMed  CAS  Google Scholar 

  • Nilsson, E., & Bengtsson, G. (2004b). Death odour changes movement pattern of a Collembola. Oikos, 104, 509–517.

    Article  Google Scholar 

  • Parejko, K., & Dodson, S. (1990). Progress towards characterization of a predator/prey kairomone: Daphnia pulex and Chaoborus americanus. Hydobiologia, 198, 51–59.

    Article  Google Scholar 

  • Peterson, S. C. (1987). Communication of leaf suitability by gregarious eastern tent caterpillars (Malacosoma americanum). Ecological Entomology, 12, 283–289.

    Article  Google Scholar 

  • Peterson, S. C., Johnson, N. D., & LeGuyader, J. L. (1987). Defensive regurgitation of allelochemicals derived from host cyanogenesis by eastern tent caterpillars. Ecology, 68, 1268–1272.

    Article  Google Scholar 

  • Pijanowska, J. (1997). Alarm signals in Daphnia? Oecologia, 112, 12–16.

    Article  Google Scholar 

  • Pijanowska, J., & Kowalczewski, A. (1997). Cues from injured Daphnia and from cyclopoids feeding on Daphnia can modify life histories of conspecifics. Hydrobiologia, 350, 99–103.

    Article  Google Scholar 

  • Pohnert, G. (2002). Phospholipase A(2) activity triggers the wound-activated chemical defense in the diatom Thalassiosira rotula. Plant Physiology, 129, 103–111.

    Article  PubMed  CAS  Google Scholar 

  • Poinar, G. O., Jr., & Danforth, B. N. (2006). A fossil bee from early cretaceous Burmese amber. Science, 314, 614.

    Article  PubMed  CAS  Google Scholar 

  • Prado, N., Marazuela, E. G., Segura, E., Fernandez-Garcia, H., Villalba, M., Thery, C., et al. (2008). Exosomes from branchoalveolar fluid of tolerized mice prevent allergic reaction. Journal of Immunology, 181, 1519–1525.

    CAS  Google Scholar 

  • Qazi, K. R., Gehrmann, U., Domange Jordo, E., Karlsson, M. C. I., & Gabrielsson, S. (2009). Antigen-loaded exosomes alone induce Th1-type memory through a B cell-dependent mechanism. Blood, 113, 2673–2683.

    Article  PubMed  CAS  Google Scholar 

  • Rittschof, D., Tsai, D. W., Massey, P. G., Blanco, L., Kueber, G. L., Jr., & Haas, R. J., Jr. (1992). Chemical mediation of behavior in hermit crabs: Alarm and aggregation cues. Journal of Chemical Ecology, 18, 959–984.

    Article  Google Scholar 

  • Rollo, C. D. (2006). Radiation and the regulatory landscape of neo2-Darwinism. Mutation Research, 597, 18–31.

    PubMed  CAS  Google Scholar 

  • Rollo, C. D., Borden, J. H., & Casey, I. (1995). Endogenously produced repellent from American cockroach (Blattaria: Blattidae): Function in death recognition. Environmental Entomology, 24, 116–124.

    Google Scholar 

  • Rollo, C. D., Czyewska, E., & Borden, J. H. (1994). Fatty acid necromones for cockroaches. Naturwissenschaften, 81, 400–410.

    Article  Google Scholar 

  • Rosenfeld, J. M. (2002). Application of analytical derivatizations to the quantitative and qualitative determination of fatty acids. Analytica Chimica Acta, 465, 93–100.

    Article  CAS  Google Scholar 

  • Rosenfeld, J. M. (2003). Derivatization in the current practice of analytical chemistry. Trends in Analytical Chemistry, 22, 785–798.

    Article  CAS  Google Scholar 

  • Shabani, S., Kamio, M., & Derby, C. D. (2008). Spiny lobsters detect conspecific blood-borne alarm cues exclusively through olfactory sensilla. Journal of Experimental Biology, 211, 2600–2608.

    Article  PubMed  Google Scholar 

  • Short, T. M., & Holomuzki, J. R. (1992). Indirect effects of fish on foraging behaviour and leaf processing by the isopod Lirceus fontinalis. Freshwater Biology, 27, 91–97.

    Article  Google Scholar 

  • Slessor, K. N., Winston, M. L., & Conte, Y. L. (2005). Pheromone communication in the honeybee (Apis mellifera L.). Journal of Chemical Ecology, 31, 2731–2745.

    Article  PubMed  CAS  Google Scholar 

  • Stabell, O. B., Ogbebo, F., & Primicerio, R. (2003). Inducible defences in Daphnia depend on latent alarm signals from conspecific prey activated in predators. Chemical Senses, 28, 141–153.

    Article  PubMed  CAS  Google Scholar 

  • Stachowicz, J. J. (2001). Chemical ecology of mobile benthic invertebrates: Predators and prey, allies and competitors. In J. B. McClintock & B. J. Baker (Eds.), Marine chemical ecology (pp. 157–194). Boca Raton, FL: CRC Press.

    Google Scholar 

  • Stout, J. C., Goulson, D., & Allen, J. A. (1998). Repellent scent-marking of flowers by a guild of foraging bumblebees (Bombus sp.). Behavioral Ecology and Sociobiology, 43, 317–326.

    Article  Google Scholar 

  • Su, N. Y. (2005). Response of the formosan subterranean termites (Isoptera: Rhinotermitidae) to baits or nonrepellent termiticides in extended foraging arenas. Journal of Economic Entomology, 98, 2143–2151.

    Article  PubMed  CAS  Google Scholar 

  • Surinov, B. P. (2007). Mice with radiation or toxic damage or malignant tumors produce aversive chemosignals repelling intact animals. Doklady Biological Sciences, 414, 199–201.

    Article  PubMed  CAS  Google Scholar 

  • Takeda, N. (1984). The aggregation phenomenon in terrestrial isopods. Symposia of the Zoological Society of London, 53, 381–404.

    Google Scholar 

  • Tollrian, R., & Harvell, C. D. (Eds.). (1999). The ecology and evolution of inducible defenses. Princeton: Princeton University Press.

    Google Scholar 

  • Traniello, J. F. A., Rosengaus, R. B., & Savoie, K. (2002). The development of immunity in a social insect: Evidence for the group facilitation of disease resistance. Proceedings of the National Academy of Sciences of the United States of America, 99, 6838–6842.

    Article  PubMed  CAS  Google Scholar 

  • Ugelvig, L. V., & Cremer, S. (2007). Social prophylaxis: Group interaction promotes collective immunity in ant colonies. Current Biology, 17, 1967–1971.

    Article  PubMed  CAS  Google Scholar 

  • Visscher, P. K. (1983). The honeybee way of death: Necrophoric behaviour in Apis mellifera colonies. Animal Behaviour, 31, 1790–1801.

    Article  Google Scholar 

  • von Elert, E., & Stibor, H. (2006). Predator-mediated life history shifts in Daphnia: Enrichment and preliminary chemical characterisation of a kairomone exuded by fish. Archiv für Hydrobiologie, 167, 21–35.

    Article  CAS  Google Scholar 

  • Williams, D. D., & Moore, K. A. (1985). The role of semiochemicals in benthic community relationships of the lotic amphipod Gammarus pseudolimnaeus: A laboratory analysis. Oikos, 44, 280–286.

    Article  Google Scholar 

  • Wilson, E. O., Durlach, N. I., & Roth, L. M. (1958). Chemical releasers of necrophoric behavior in ants. Psyche, 65, 108–114.

    Article  Google Scholar 

  • Wilson, E. O., & Hölldobler, B. (2005). The rise of the ants: A phylogenetic and ecological explanation. Proceedings of the National Academy of Sciences of the United States of America, 102, 7411–7414.

    Article  PubMed  CAS  Google Scholar 

  • Wilson-Rich, N., Spivak, M., Fefferman, N. H., & Starks, P. T. (2009). Genetic, individual, and group facilitation of disease resistance in insect societies. Annual Review of Entomology, 54, 405–423.

    Article  PubMed  CAS  Google Scholar 

  • Wisenden, B. D. (2003). Chemically mediated strategies to counter predation. In S. P. Collin & N. J. Marshall (Eds.), Sensory processing in aquatic environments (pp. 236–251). New York: Springer.

    Chapter  Google Scholar 

  • Wisenden, B. D., Chivers, D. P., & Smith, R. J. F. (1997). Learned recognition of predation risk by Enallagma damselfly larvae (Odonata, Zygoptera) on the basis of chemical cues. Journal of Chemical Ecology, 23, 137–151.

    Article  CAS  Google Scholar 

  • Wisenden, B. D., Pohlman, S. G., & Watkin, E. E. (2001). Avoidance of conspecific injury-released chemical cues by free-ranging Gammarus lacustris (Crustacea: Amphipoda). Journal of Chemical Ecology, 27, 1249–1258.

    Article  PubMed  CAS  Google Scholar 

  • Worden, B. D., & Parker, P. G. (2005). Females prefer noninfected males as mates in the grain beetle Tenebrio molitor: Evidence in pre- and postcopulatory behaviours. Animal Behaviour, 70, 1047–1053.

    Article  Google Scholar 

  • Wudkevich, K., Wisenden, B. D., Chivers, D. P., & Smith, R. J. F. (1997). Reactions of Gammarus lacustris to chemical stimuli from natural predators and injured conspecifics. Journal of Chemical Ecology, 23, 1163–1173.

    Article  CAS  Google Scholar 

  • Zar, J. H. (1974). Biostatistical analysis. Engelwood Cliffs, NJ: Prentice Hall.

    Google Scholar 

  • Zimmer-Faust, R. K., Tyre, J. E., & Case, J. F. (1985). Chemical attraction causing aggregation in the spiny lobster Panulirus interruptus (Randall) and its probable ecological significance. Biological Bulletin, 169, 106–118.

    Article  Google Scholar 

  • Zulandt Schneider, R. A., & Moore, P. A. (2000). Urine as a source of conspecific disturbance signals in the crayfish Procambarus clarkia. Journal of Experimental Biology, 203, 765–771.

    PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by the Natural Sciences and Engineering Research Council of Canada. Mary Ann dela Cruz, Melanie Prosser, Tara Ladd, and Cathy Woods contributed to the research effort. I thank our editor, Dr. Benedikt Hallgrimsson and two anonymous reviewers who greatly improved this paper.

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Yao, M., Rosenfeld, J., Attridge, S. et al. The Ancient Chemistry of Avoiding Risks of Predation and Disease. Evol Biol 36, 267–281 (2009). https://doi.org/10.1007/s11692-009-9069-4

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