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The Ancient Chemistry of Avoiding Risks of Predation and Disease

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

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

    Article  Google Scholar 

  2. 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 

  3. 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.

    PubMed  Article  Google Scholar 

  4. 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 

  5. 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 

  6. 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 

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

    PubMed  Article  CAS  Google Scholar 

  8. 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 

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

    PubMed  Article  CAS  Google Scholar 

  10. 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 

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

    Google Scholar 

  12. 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 

  13. 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.

    PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

  15. 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 

  16. 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.

    PubMed  Article  Google Scholar 

  17. 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 

  18. 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 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  21. 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.

    PubMed  Article  CAS  Google Scholar 

  22. 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 

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

    Google Scholar 

  24. 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 

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

    Article  Google Scholar 

  26. 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 

  27. 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 

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

    PubMed  Article  CAS  Google Scholar 

  29. 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 

  30. 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.

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  34. 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.

    PubMed  Article  CAS  Google Scholar 

  35. 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 

  36. 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.

    PubMed  Article  Google Scholar 

  37. 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 

  38. 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 

  39. 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 

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

    Article  CAS  Google Scholar 

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

    PubMed  Article  Google Scholar 

  42. 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.

    PubMed  Article  CAS  Google Scholar 

  43. 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.

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  45. 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 

  46. 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 

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

    Google Scholar 

  48. 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.

    PubMed  Article  CAS  Google Scholar 

  49. 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 

  50. 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 

  51. 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 

  52. 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 

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

    PubMed  Article  CAS  Google Scholar 

  54. 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 

  55. 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 

  56. 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 

  57. 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.

    PubMed  Article  CAS  Google Scholar 

  58. 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 

  59. 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.

    PubMed  Article  CAS  Google Scholar 

  60. 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 

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

    PubMed  Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  63. 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 

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

    Article  Google Scholar 

  65. 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 

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

    Article  Google Scholar 

  67. 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 

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

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  70. 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 

  71. 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.

    PubMed  Article  CAS  Google Scholar 

  72. 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 

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

    PubMed  CAS  Google Scholar 

  74. 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 

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

    Article  Google Scholar 

  76. 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 

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

    Article  CAS  Google Scholar 

  78. 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.

    PubMed  Article  Google Scholar 

  79. 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 

  80. 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.

    PubMed  Article  CAS  Google Scholar 

  81. 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.

    PubMed  Article  CAS  Google Scholar 

  82. 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 

  83. 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 

  84. 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.

    PubMed  CAS  Article  Google Scholar 

  85. 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.

    PubMed  Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  88. 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.

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  91. 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 

  92. 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 

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

    Article  Google Scholar 

  94. 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.

    PubMed  Article  CAS  Google Scholar 

  95. 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.

    PubMed  Article  CAS  Google Scholar 

  96. 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 

  97. 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 

  98. 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.

    PubMed  Article  CAS  Google Scholar 

  99. 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 

  100. 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 

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

    Google Scholar 

  102. 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 

  103. 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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Correspondence to C. D. Rollo.

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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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Keywords

  • Isopoda
  • Caterpillars
  • Death recognition
  • Shelter selection
  • Necromones
  • Behavior
  • Predation
  • Disease
  • Fatty acids