Animal Weapons

by Douglas J. Emlen

  Clever and Selfo came through for me that night. I’m sure they were terrified I would die on their watch, sinking their fledgling outfitter business in the process, but they risked their boat and their lives getting me to medicine. The Napo in those days had a “shoot-on-sight” curfew after dark—part of the war on drugs. Thick mist over the water helped hide our boat, but navigating around sandbars and snags without lights is dicey. I was delirious most of the trip, though I remember looking up at one point as a huge floating tree whooshed by in the darkness.

  2. L. G. Nico and D. C. Taphorn, “Food Habits of Piranhas in the Low Llanos of Venezuela,” Biotropica 20 (1988): 311–21; V. L. de Almeida, N. S. Hahn, and C. S. Agostinho, “Stomach Content of Juvenile and Adult Piranhas (Serrasalmus marginatus) in the Paraná Floodplains, Brazil,” Studies on Neotropical Fauna and Environment 33 (1998): 100–105.

  3. J. H. Mol, “Attacks on Humans by the Piranha Serrasalmus rhombeus in Suriname,” Studies on Neotropical Fauna and Environment 41 (2006): 189–195.

  4. F. Juanes, J. A. Buckel, and F. S. Scharf, “Feeding Ecology of Piscivorous Fishes,” in Handbook of Fish Biology and Fisheries, ed. P. J. B. Hart and J. D. Reynolds (Malden, MA: Blackwell Publishing, 2002); J. R. Grubich, A. N. Rice, and M. W. Westneat, “Functional Morphology of Bite Mechanics in the Great Barracuda (Sphyraena barracuda),” Zoology 111 (2008): 16–29.

  5. H. B. Owre and F. M. Bayer, “The Deep-Sea Gulper Eurypharynx pelecanoides Vaillant 1882 (Order Lyomeri) from the Hispaniola Basin,” Bulletin of Marine Science 20 (1970): 186–92; J. G. Nielsen, E. Bertelsen, and A. Jespersen, “The Biology of Eurypharynx pelecanoides (Pisces, Eurypharyngidae),” Acta Zoologica 70 (1989): 187–97.

  6. Gavin J. Svenson and Michael F. Whiting, “Phylogeny of Mantodea Based on Molecular Data: Evolution of a Charismatic Predator,” Systematic Entomology 29 (2004): 359–70.

  7. H. Maldonado, L. Levin, and J. C. Barros Pita, “Hit Distance and the Predatory Strike of the Praying Mantis,” Zeitschrift Für Vergleichende Physiologie 56 (1967): 237–57; Taku Iwasaki, “Predatory Behavior of the Praying Mantis, Tenodera aridifolia II. Combined Effect of Prey Size and Predator Size in the Prey Recognition,” Journal of Ethology 9 (1991): 77–81; R. G. Loxton and I. Nicholls, “The Functional Morphology of the Praying Mantis Forelimb (Dictyoptera: Mantodea),” Zoological Journal of the Linnean Society 66 (2008): 185–203.

  8. Sheila N. Patek, W. L. Korff, and Roy L. Caldwell, “Deadly Strike Mechanism of a Mantis Shrimp,” Nature 428 (2004): 819–20.

  9. D. Lohse, B. Schmitz, and M. Versluis, “Snapping Shrimp Make Flashing Bubbles,” Nature 413 (2001): 477–78.

  10. Beautiful studies of the genetics of caste development reveal how chemical cues interact with developmental hormones to regulate the expression of genes in ways that are specific to each caste, coordinating the details of their growth. For example, Ehab Abouheif and Greg A. Wray, “Evolution of the Genetic Network Underlying Wing Polyphenism in Ants,” Science 297 (2002): 249–52; Julia H. Bowsher, Gregory A. Wray, and Ehab Abouheif, “Growth and Patterning Are Evolutionarily Dissociated in the Vestigial Wing Discs of Workers of the Red Imported Fire Ant, Solenopsis invicta,” Journal of Experimental Zoology, Part B: Molecular and Developmental Evolution 308 (2007): 769–76. There are also a number of excellent studies of the effects of nutrition and hormones on caste development, such as Diana E. Wheeler, “The Developmental Basis of Worker Caste Polymorphism in Ants,” American Naturalist (1991): 1218–38.

  11. Sheila N. Patek, J. E. Baio, B. L. Fisher, and A. V. Suarez, “Multifunctionality and Mechanical Origins: Ballistic Jaw Propulsion in Trap-Jaw Ants,” Proceedings of the National Academy of Sciences 103 (2006): 12787–92.

  12. Olivia I. Scholtz, Norman Macleod, and Paul Eggleton, “Termite Soldier Defence Strategies: A Reassessment of Prestwich’s Classification and an Examination of the Evolution of Defence Morphology Using Extended Eigenshape Analyses of Head Morphology,” Zoological Journal of the Linnean Society 153 (2008): 631–50.

  13. Trevor N. Dupuy, The Evolution of Weapons and Warfare (New York: Da Capo Press, 1984); R. L. O’Connell, Of Arms and Men: A History of War, Weapons, and Aggression (Oxford: Oxford University Press, 1989); M. van Creveld, Technology and War: From 2000 B.C. to the Present (New York: Free Press, 1989); O’Connell, Soul of the Sword: An Illustrated History of Weaponry and Warfare from Prehistory to the Present (New York: Free Press, 2002).

  14. Robert L. O’Connell, Sacred Vessels: The Cult of the Battleship and the Rise of the U.S. Navy (Oxford: Oxford University Press, 1991); Robert Jackson, Sea Warfare: From World War I to the Present (San Diego: Thunder Bay Press, 2008).

  4. Competition

  1. I’d put the bond between father and son to a pretty good test the week before. While my dad was in town I dragged the canoe from its hiding place in the grass by the tree and canoed to the territories alone, keeping up the jacana vigil. Crosswinds were stiff that morning, and I’d had to kneel low in the middle of the boat, paddling as hard as I could to fight the gale and keep the boat on course. As I tucked in beside one of the territories I came into the lee of tall trees on the far shore, and the wind died. I dropped anchor, assembled the tripod and scope, and set to work, bare feet tucked beneath the bench seat, knees splayed to stabilize my weight in the bottom of the boat. Black flies had been everywhere that week, and it didn’t take long before I felt the telltale tickle of one crawling up my calf. I’m still not sure why I bothered to look, since flies can be swatted without taking your eye from the scope. But I did look, and I flinched. Crawling up my bare leg was a tarantula, not a fly. Six inches of spider! I admit it; I reacted badly. I jumped, the canoe rocked, and a thousand dollars’ worth of tripod and scope flipped over the side, vanishing forever into the swift muddy deep.

  2. C. Yeung, M. Anapolski, M. Depenbusch, M. Zitzmann, and T. Cooper, “Human Sperm Volume Regulation: Response to Physiological Changes in Osmolality, Channel Blockers, and Potential Sperm Osmolytes,” Human Reproduction 18 (2003): 1029.

  3. J. Rutkowska and M. Cichon, “Egg Size, Offspring Sex, and Hatching Asynchrony in Zebra Finches, Taeniopygia guttata,” Journal of Avian Biology 36 (2005): 12–17.

  4. W. A. Calder, C. R. Pan, and D. P. Karl, “Energy Content of Eggs of the Brown Kiwi, Apteryx australis; an Extreme in Avian Evolution,” Comparative Biochemistry and Physiology Part A: Physiology 60 (1978): 177–79.

  5. L. W. Simmons, R. C. Firman, G. Rhodes, and M. Peters, “Human Sperm Competition: Testis Size, Sperm Production and Rates of Extrapair Copulations,” Animal Behaviour 68 (2004): 297–302.

  6. Another reason parental care is generally provided by females, rather than males, has to do with the certainty of parentage. For many animal species females retain the eggs inside their bodies until after they are fertilized. A female who cares for these eggs can be certain that they are hers, and not those of another female, so energy and time invested are well spent. Males have no such assurance, for precisely the same reason: if fertilization happens inside females then males run the risk that sperm from a rival male actually fertilizes the offspring. Expending resources for the care of unrelated offspring is not cost-effective. Consequently, because females have invested the most already, and because they generally have higher certainty of genetic parentage than their mates, selection favors the evolution of maternal care of offspring more often than it does paternal care.

  7. Cockroaches actually show all sorts of interesting forms of parental care. A good review is provided by Christine Nalepa and William Bell, “Postovulation Parental Investment and Parental Care in Cockroaches,” in The Evolution of Social Behavior in Insects and Arachnids, ed. Jae Choe and Bernard Crespi (Cambridge: Cambridge University Press, 1997), 26–51.

  8. T. G. Benton, “Reproduction and Parental Care in the Scorpion, Euscorpius flavicaudis,” Behaviour 117 (1991): 20–29.

  9. G. Halffter and W. D. Edmonds, The Nesting Behavior of Dung Beetles (Scarabaeinae): An Ecological and Evolutive Approach (
Mexico, D.F.: Instituto de Ecologia, 1982).

  10. The concept described here is called the “operational sex ratio” (OSR). Whereas the sex ratio is simply a head count of the number of males and females in a population (and, in all but a very few exceptional species, this ratio hovers near 1:1), the operational sex ratio accounts for the fact that not all individuals are actually available for reproducing at any point in time. It is defined as the ratio of reproductively available males to reproductively available females. The OSR can skew in the direction of females, as it does in jacanas, but it is typically skewed toward an excess of available males. The extent of skew is a good metric for the intensity of sexual selection likely to be acting in the population. The foundational paper describing this concept was written by my father, Stephen Emlen, and Lewis Oring, “Ecology, Sexual Selection, and the Evolution of Mating Systems,” Science 197 (1977): 215–23. A more recent twist on these concepts is provided by H. Kokko and P. Monaghan, “Predicting the Direction of Sexual Selection,” Ecology Letters 4 (2001): 159–65.

  11. C. Darwin, The Descent of Man and Selection in Relation to Sex (London: John Murray, 1871).

  12. S. T. Emlen and P. H. Wrege, “Size Dimorphism, Intrasexual Competition, and Sexual Selection in the Wattled Jacana (Jacana jacana), a Sex-Role-Reversed Shorebird in Panama,” Auk 121 (2004): 391–403; Emlen and Wrege, “Division of Labor in Parental Care Behavior of a Sex-Role-Reversed Shorebird, the Wattled Jacana,” Animal Behaviour 68 (2004): 847–55.

  13. If you’re wondering why it’s the male who cares for the young in this species, that’s a question my dad spent all those years answering, and a topic for a different book. But I can refer you to his paper: Emlen and Wrege, “Division of Labor in Parental Care Behavior,” 847–55.

  14. J. H. Poole, “Mate Guarding, Reproductive Success, and Female Choice in African Elephants,” Animal Behaviour 37 (1989): 842–49.

  15. Ibid.

  16. J. A. Hollister-Smith, J. H. Poole, E. A. Archie, E. A. Vance, N. J. Georgiadis, C. J. Moss, and S. C. Alberts, “Age, Musth, and Paternity Success in Wild Male African Elephants, Loxodonta Africana,” Animal Behaviour 74 (2006): 287–96.

  17. H. F. Osborn, “The Ancestral Tree of the Proboscidea: Discovery, Evolution, Migration, and Extinction over a 50,000,000 Year Period,” Proceedings of the National Academy of Sciences 21 (1935): 404–12; J. Shoshani and T. Pascal, eds., The Proboscidea: Evolution and Paleoecology of Elephants and Their Relatives (Oxford: Oxford University Press, 1993); W. J. Sanders, “Proboscidea,” in Paleontology and Geology of Laetoli: Human Evolution in Context, vol. 2, Fossil Hominins and the Associated Fauna, ed. T. Harrison (New York: Springer, 2011).

  18. F. Kottenkamp, History of Chivalry and Ancient Armour (London: Willis and Sotheran, 1857); G. Duby, The Chivalrous Society, trans. Cynthia Poston (Berkeley: University of California Press, 1977); R. L. O’Connell, Of Arms and Men: A History of War, Weapons, and Aggression (Oxford: Oxford University Press, 1989); J. France, Western Warfare in the Age of the Crusades, 1000–1300 (Ithaca, NY: Cornell University Press, 1999).

  19. Duby, Chivalrous Society.

  20. Ibid.

  21. Ibid.

  22. Ibid.

  23. Ibid.

  24. Ibid.

  25. Ibid.

  26. Ibid.

  27. Ibid.

  28. Duby, Chivalrous Society; O’Connell, Of Arms and Men.

  29. O’Connell, Of Arms and Men.

  30. Duby, Chivalrous Society; O’Connell, Of Arms and Men.

  31. Kottenkamp, History of Chivalry and Ancient Armour; O’Connell, Of Arms and Men.

  32. Reproduction outside of marriage was also tied with rank and wealth. To an extraordinary degree, powerful lords sequestered young women inside the walls of their castles, plucking them from their homesteads to work as maids and attendants. There is abundant evidence that these lords mated prolifically with harems of these women, often siring dozens of illegitimate children. In some cases, they prevented these women from marrying other men; in others, they sequestered them as virgins, and then married them off after they had had a child with the castle lord. For a comprehensive treatment of these issues, I recommend the writings of Laura Betzig, including “Medieval Monogamy,” Journal of Family History 20 (1995): 181–216; and Despotism and Differential Reproduction: A Darwinian View of History (Hawthorne, NY: Aldine, 1986).

  33. Michael Bell, Jeffrey Baumgartner, and Everett Olson, “Patterns of Temporal Change in Single Morphological Characters of a Miocene Stickleback Fish,” Paleobiology 11 (1985): 258–71.

  34. A fantastic illustration of this is the long-term study of bill evolution in Galapagos finches conducted by Peter and Rosemary Grant. For more than forty years they measured natural selection and evolution of beak shape in a population of seed-eating ground finches living on the tiny island of Daphne Major. Birds with thick beaks were better at cracking large, tough seeds, while those with slender beaks were faster at feeding on tiny seeds. The Grants showed that year-to-year fluctuations in rainfall led to dramatic shifts in the types and amounts of seeds available to the birds, and this resulted in selection favoring deep beaks in some years but thin beaks in others. Although natural selection was directional and strong for most years of this period, the pattern of selection oscillated, so that the net effect was stasis. Despite multiple bouts of rapid change, birds at the end of the sample period had roughly the same bill shapes as those at the beginning. The first thirty years of this study are described in Peter Grant and Rosemary Grant, “Unpredictable Evolution in a 30-Year Study of Darwin’s Finches,” Science 296 (2002): 707–11.

  35. Charles Darwin first recognized this special property of sexual selection in The Descent of Man and Selection in Relation to Sex (London: John Murray, 1871), but the logic of escalation and unending change was best (and beautifully) articulated in two papers by Mary Jane West Eberhard, “Sexual Selection, Social Competition, and Evolution,” Proceedings of the American Philosophical Society 123 (1979): 222–34; and “Sexual Selection, Social Competition, and Speciation,” Quarterly Review of Biology 58 (1983): 155–83.

  36. I should add the caveat “adult” animals, as in many species juvenile mortality is severe, and selection for traits that facilitate survival to the age of reproduction is just as strong, or even stronger, than selection for traits involved in reproduction. For an example of this, see the studies of natural and sexual selection in water striders by Daphne Fairbairn, such as R. F. Preziosi and D. J. Fairbairn, “Lifetime Selection on Adult Body Size and Components of Body Size in a Waterstrider: Opposing Selection and Maintenance of Sexual Size Dimorphism,” Evolution 54 (2000): 558–66.

  5. Economic Defensibility

  1. Much of the work on túngara frogs has been conducted by Michael Ryan. See, for example, his book The Túngara Frog: A Study in Sexual Selection and Communication (Chicago, University of Chicago Press, 1992); or his paper “Female Mate Choice in a Neotropical Frog,” Science 209 (1980): 523–25.

  2. An absolutely gorgeous book on birds of paradise is Tim Layman and Edwin Scholes, Birds of Paradise: Revealing the World’s Most Extraordinary Birds (Washington, DC: National Geographic, 2012). Early studies of female choice in these birds were conducted by Stephen Pruett-Jones and his students. See, for example, S. G. Pruett-Jones and M. A. Pruett-Jones, “Sexual Selection Through Female Choice in Lawes’ Parotia, a Lek-Mating Bird of Paradise,” Evolution 44 (1990): 486–501.

  3. The concept of female choice traces to Darwin (The Descent of Man and Selection in Relation to Sex, London: John Murray, 1871), and this aspect of sexual selection has been the focus of literally thousands of empirical studies in all sorts of interesting species. A good place to start delving into this topic is the overview of sexual selection provided by Malte Andersson, Sexual Selection (Princeton, NJ: Princeton University Press, 1994).

  4. My colleagues and I used information from the DNA sequences of approximately fifty species of the dung beetle genus Onthophagus to arrange taxa i
nto a nested series of groups based on their relatedness. The resulting tree, called a phylogeny, describes the history of these animals and can be used to trace the evolution of particular traits such as horns. This study showed that horns were gained and lost repeatedly in the history of these beetles. D. J. Emlen, J. Marangelo, B. Ball, and C. W. Cunningham, “Diversity in the Weapons of Sexual Selection: Horn Evolution in the Beetle Genus Onthophagus (Coleoptera: Scarabaeidae),” Evolution 59 (2005): 1060–84.

  5. Ilkka Hanski and Yves Cambefort, eds., Dung Beetle Ecology (Princeton, NJ: Princeton University Press, 1991), provides a readable and comprehensive account of the geographical distribution of dung beetles, as well as their evolutionary history.

  6. A great treatment of these topics is provided in chapters 8 and 11 of John Alcock, Animal Behavior, 8th ed. (Sunderland, MA: Sinauer Associates, 2005). A classic paper applying these concepts to sexual selection and the evolution of animal behavior is the paper by my father, Stephen Emlen, and Lewis Oring, “Ecology, Sexual Selection, and the Evolution of Mating Systems,” Science 197 (1977): 215–23.

  7. Jeanne and David Zeh describe their adventures in Panamanian forests in search of harlequin beetles in “Tropical Liaisons on a Beetle’s Back,” Natural History (1994): 36–43. Their results are published in the article “Sexual Selection and Sexual Dimorphism in the Harlequin Beetle Acrocinus longimanus,” Biotropica 24 (1992): 86–96.

  8. The Zehs’ work on pseudoscorpions is published in the papers “Dispersal-Generated Sexual Selection in a Beetle-Riding Pseudoscorpion,” Behavioral Ecology and Sociobiology 30 (1992): 135–42, and “Sex Via the Substrate: Sexual Selection and Mating Systems in Pseudoscorpions,” in The Evolution of Mating Systems in Insects and Arachnids, ed. J. C. Choe and B. J. Crespi (Cambridge: Cambridge University Press, 1997): 329–39. Much of their recent work focuses on these tiny arthropods. Now that they have developed methods for rearing them in captivity in their laboratory, the Zehs have looked extensively at the genetic benefits that female pseudoscorpions derive from mating with dominant males on the backs of beetles, and from mating with several different males as they ride on beetle after beetle. See, for example, their paper “Genetic Benefits Enhance the Reproductive Success of Polyandrous Females,” Proceedings of the National Academy of Sciences 96 (1999): 10236–41.