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Religious supplicant, seductive cannibal, or reflex machine? In search of the praying mantis

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Conclusion

The original, prescientific Western belief that the mantis is a pious, helpful creature became a widely held explanation for the mantid's unique resting (apparently prayerful) posture, and for one of its cryptic displays (extending the forelegs straight out). This belief was a characteristic part of a broader discourse about nature in which ancient authority, religious beliefs, and superstition, but few original observations, mixed freely. Gradually, the belief in mantid gentleness and piousness became a commonplace through the continual retelling of the myths and superstitions surrounding this fascinating insect.

By the seventeenth century, a growing interest in observation had begun to replace blind reliance on established wisdom and ancient authority. However, the various young sciences to which the period gave rise did not progress equally, and neither did the subdisciplines within each scientific field; biology, especially entomology, was particularly slow to free itself from past beliefs and contemporary superstitions. In the specific case of the praying mantis, the situation may have been at its worst.

Early observers of nature found evidence that seemed, at first, to disconfirm the well-established belief that mantids are gentle creatures. These few observers, faced with startling firsthand information about mantid voraciousness, created a new characterization of mantids as merciless predators and then often juxtaposed the two images in their descriptions. However, it was not until the beginning of the nineteenth century that the two characterizations-gentleness versus cruelty—became reconciled.

An amalgamation of these seemingly mutually exclusive characterizations was achieved by an interesting accommodation of each to the other. That is, while it could no longer be maintained that mantids are simply gentle insects, neither could it be accepted that they are all cruelty and viciousness. The melding of the two characterizations yielded a hybrid explanation which claimed that the praying mantis actually hastwo sides to its character! On the one hand, and like other creatures, mantids must nourish themselves, and do so quite reasonably by capturing small insects for food. However, even when “well nourished,” and without “the excuse of hunger,” their other, vicious side may surface; when this happens, the darkest of behaviours, cannibalism, is the result.

To understand the remainder of the story one must pause to consider what had happened in the other sciences up to this point. In the mid-seventeenth century, professional scientific societies (such as the Royal Society of London, the Académic Royale des Sciences in France, and the Accademia del Cimento in Florence) were established throughout Europe. The societies, and the various journals and periodicals that they produced or encouraged, represented an institutionalization of both science and its special, structured discourse. However, as we have stated, entomology lagged behind; and in the case of some insects, superstitions and anthropomorphisms did not fade from descriptions of their behavior for centuries to come.

By the time the new scientific discourse was applied to mantids the creatures were already firmly shackled with a dual personality, and this assumption was never challenged. In fact, it was functionally impossible to disconfirm. Captures of small prey were considered part of the mantid's normal side; captures of large prey (including conspecifics) were considered part of the mantid's abnormal side. There was no alternative explanation.

As luck would have it, by the time that the strictures of scientific discourse had tightened sufficiently to disallow the use of anthropomorphisms in the explanation of insect behavior, another acceptable explanation of mantid cannibalism became immediately available: cannibalism became part of mantid mating behavior. That is, the fundamental explanatory model remained unchanged; it was merely couched in more appropriate terms. The acceptance of this new explanation for cannibalism was virtually immediate and complete. For instance, no one ever asked the following questions: If the headless male remains able to mate as a putative precaution against female cannibalism, for what reason does the headless female remain able to fashion “a perfectly constructed ootheca”? Or: If female-on-male cannibalism plays a role in mating behavior, what role is played by genderindifferent cannibalism, especially that among immature mantids? The latter phenomena were simply ignored — they were just uninteresting artifacts of insect life. However, the grand logic of nature was immediately apparent in the headless male's ability to mate. The ruling theory, to use Chamberlin's term, had been able to accommodate itself to, and assimilate, the new scientific discourse. It remained unscathed.

A persistent question posed by several historians of this particular topic has been, Why did not the results of Ken Roeder's experiments debunk the myth that males are regularly cannibalized by the females with which they mate? The reason, which we hope is now clear, is that there were (and are) two interdependent ruling theories operating here. If one accepts the argument that mantids' cannibalism is simply a normal part of their prey-catching behavior, then one attacks not only the theory that mantids have two separate predatory strategies, but also the more recent theory that mantids have evolved to be the ideal fly-catching machines. This second theory found its first confirming support in the centuries-old (fortuitous) practice of feeding flies to captive mantids. Again, the disconfirming evidence of mantids eating prey of various sizes had no impact on the theory. Confirming observations were accepted: disconfirming observations were seen as anomalies.

Additional confirmation of both ruling theories was garnered in experiments done in the mid-twentieth century. These experiments were based on the assumption that the original conceptualizations were correct, and consequently they did not test other hypotheses. The combined strength of the two theories is evidenced especially in the Raus' failure to account for the fact that their empirical observations were at odds with many of the conclusions that they drew, and in the fact that Roeder's work is still used to support the belief in the regularity (or necessity) of mating-related cannibalism despite the fact that Roeder, himself, argued the opposite. with both theories well entrenched, it is virtually impossible to promote an alternative theory of mantid behavior: namely, that mantids are generalized, opportunistic predators that manage to survivein spite of the fact that cannibalism sometimes occurs.

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References

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  31. Among these physician/entomologists was the English doctor Edward Wotton (1492–1555). Wotton is known primarily for his workDe differentiis animalium libri decem, published in Paris in 1552. The work is divided into ten books, the ninth dealing with insects. However, it contains no new information; its strength is that it is an early objective summary of the ancient Graeco-Roman entomological literature. Although Wotton's book did not see a second printing, it is considered to be the beginning of the Aristotelian Renaissance in Zoology. Many popular, secular, and theologically oriented works appeared during the period, but, like Wotton's text, none offered any new, or even much accurate, information about insects. See MaxBeier, “The Early Naturalists and Anatomists during the Renaissance and Sevententh Century,” in ed. Ray F.Smith, Thomas E.Mittler, and Carroll N., SmithHistory of Entomology (Palo Alto, Calif.: Annual Reviews, 1973), pp. 82–85.

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  34. Aldrovandi studied Gesner's work diligently but is thought by some to have been neither as criticial nor as good a stylist as was Gesner (ErikNordenskiöld,The History of Biology [New York: Tudor, 1928], p. 95). Aldrovandi came to be seen simply as a compiler, for which he has been harshly (and perhaps undeservedly) criticized. For instance, the naturalist Georges-Louis Leclerc, Comte de Buffon (1707–88), said that nine-tenths of Aldrovandi's work is useless and untrue, and Cuvier (1769–1832) referred to it as “an undigested and wearisome compilation” (cited in James Wilson,A Treatise on Insects [Edinburgh: Adam and Charles Black, 1835], p. 5). On the other hand, Max Beier has argue that Aldrovandi was the superior entomologist (Beier, “Early Naturalists,” p. 86).

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  38. August Johann Rösel von Rosenhof (sometimes referred to as Roesel) was a successful portrait painter who became enthralled with painting insects and describing their habits after seeing the work of Maria Slbylla Merian (1647–1717). Merian was the first person to undertake an expedition solely for the purpose of entomological research. She produced several volumes of work containing beautiful plates of insects and their habitats. Her best-known works areMetamorphosis Insectorum Surinamensis (Amsterdam, 1705) andHistoire des Insectes de l'Europe (Amsterdam: Jean Frederic Bernard, 1730); in the former she depicted two species of mantid in plate 27. Rösel von Rosenhof produced the finely illustrated, four-volume entomological workInsecten Belustigungen (Nürnberg, 1746–61). A fifth, supplementary volume,Beytraege zur Natur oder Insecten Geschichte (Nürnberg, 1761) was brought to publication by his son-in-law, F. C. Christian Kleeman (1735–89).

  39. This account of Rösel's findings is based on several translations including (but not limited to) those inThe Natural History of Insects (London: John Murray, 1835), II, 165–169; Baron Cuvier,Animal Kingdom, (London: Gilbert and Rivington, 1832), XV, 189; and Philip Henry Gosse,Zoology, 2nd ed. (London: Society for Promoting Christian Knowledge, 1857), II, 331–333.

  40. JohnBarrow,Travels in China (London: T. Cadwell and W. Davis, 1804, 1806). Several translated editions of this widely read book were also published in France between 1804 and 1896, and in Germany in 1805. We have relied on the American edition of the text (Philadelphia: W. F. McLaughlin, 1805), pp. 106–108.

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  42. Ibid. Although Barrow does not identify the species of insects he saw fighting all subsequent commentators believed them to be mantids. As noted earlier, mantids were originally thought to be a type of locust. Insect fighting in China was also recounted inTravels in Kamtschatka by Dobell, which is cited in A. H. Swinton,Insect Variety: Its Propagation and Distribution (London: Cassell, Petter, Galpin, 1880), pp. 48–49.

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  45. The juxtaposition of these two opposing views of the mantis — one charming or beneficial, the other frightening or evil — occurs throughout popular literature extending through the nineteenth and twentieth centuries. Consider the following three examples. In the article “A Queer Pet,” Elizabeth Bellamy wrote, regarding a pet mantid: “Once, for ten summer days, I had the pleasure of entertaining a strange and most interesting guest” — but she also admitted, “I have a horror of the creature, and prefer not to touch it” (Pop. Sci. Mon., 37 [1890], 528–529). A century later, on May 13, 1990, the Arlington Heights, Ill.,Daily Herald ran a story written by Carolyn Hill for theChristian Science Monitor News Service entitled, “Is Bug-Eyed Praying Mantis a Sentry or Mini-Monster?” The author related, on the one hand, her infatuation with the mantids in her garden (“My husband and I both developed a real fascination for our new friends”), but she also admitted her fear of the creatures (“neither would admit to the other we weren't interested in doing any hand feeding”). Finally, consider these lines from the poem “The Praying Mants Visits a Penthouse” by Oscar Williams: “The praying mantis with its legs of straw / Out of nowhere's forehead born full armed / Engages the sentry at my terrace door. / Focused at inches the dinosaur insect sends / Broadsides of epic stillness at my eye, / ... / My love who fears the thunder of its poise, / Has seen it and cries out ... / I strike, the stick whistles, shearing off two legs / Which run off by themselves ... / All sinews doubtless screaming insect death. / ... / I search my mind for possible wounds and feel / The victim's body heavy on the visitor's heart” (A Little Treasury of Modern Poetry [New York: Scribners, 1950], p. 416).

  46. GeorgeShaw,General Zoology (London: for G. Kearley, 1806), pp. 117–121. Having raised several species of mantid ourselves, we must say that we have never seen a mantis cleave another through, as Rösel suggests. An account similar to Shaw's appears in Thomas Smith,The Naturalist's Cabinet (London: James cundee, 1807), VI, 288–290. In addition to the information gleaned from Moffett and from James Smith'sTour on the Continent, Thomas Smith elaborated an additional characteristic, stealth: “If it see an insect a little beyond its reach, over its head, it slowly erects its long thorax...then resting on its posterior legs, it gradually raises the anterior part also...Should the insect go from the spot, it flies or crawls after it slowly on the ground like a cat; and, when the insect stops, erects itself as before” (pp. 289–290).

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  50. A recounting of Rösel's comments inNatural History of Insects (above, n. 40), II, 168 and 166 respectively. Among the usual citations on mantis behavior is numbered Barrow's account of mantis fighting in China.

  51. “The Mantis,”The Penny Magazine of the Society for the Diffusion of Useful Knowlege (London: Charles Knight, 1841), p. 436 (italics added). In this article, the author notes that myths of mantid divinity are prevalent among the rural French, the Turks, the Muslims, the Africans, and the South Americans. In contrast to these beliefs, the remarks of Barrow, Smith, and Rösel are presented.

  52. JamesDuncan,Entomology, vol. XXXI of WilliamJardine, ed.The Naturalist's Library (Edinburgh: W. H. Lizars, 1843), p. 229. Of interest is the fact that a strange mistake about mantis behavior appears in this volume, attributed originally to the seventh edition of theEncyclopedia Britannica; the mistaken claim is that mantids “are perpetually moving their arms or forelegs in the air, and closing one armed joint upon another, so that whatever insect prey comes within reach, is immediately transfixed and consumed” (p. 229). This and several other comments suggest that the author has never himself observed a living specimen. An interesting article of similar tone entitled “Insect Appetite” appeared in the British magazineOnce A Week, 4 (1861), 300–301; although mantids are not mentioned specifically, the general impression that many insects are insatiable eaters is clearly indicated: “Some insects are endowed with an appetite so keen... that they eat incessantly ... Their existence is a feast, without a change of plates, or a pause between the courses.... Breakfast commences with infancy, and their only after-dinner nap is a passage to another state of existence.”

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  53. AchetaDomestica (Rev. J. G. Wood),Insect Life (London Bell and Daldy, 1867), p. 265.

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  54. Because this is a critical point for our overall argument, we wish to offer several corroborative examples: “Not being aware if there is any instance on record of the hatching of any species ofMantis in England, I beg to inform you that... I was much gratified by the sight of a very lively little specimen in a tumbler glass... in pursuit of small flies... [upon which]... it fed readily for about fifteen days... [In Melbourne] it is a common practice to place specimens of theMantis on the window blinds, where they keep the room clear of flies” (HenryDenny, “Hatching of theMantis in England,”Mag. Nat. Hist., 19 [1867], 144); Fig. 465 in William B. Carpenter,Zoology (London: Bell and Daldy, 1867), p. 146, depicts a “Mantis, in the act of seizing a fly...,”; “But only let an imprudent fly come within reach of our devotee, and you will see it stealthily approach it, like a cat who is watching a mouse” (Louis Figuier,The Insect World [New York: Appleton 1869], pp. 288–289); “This perfect quietude does not raise any suspicions... but if an unfortunate fly comes too close theMantis extends its foot rapidly and too surely” (P. Martin Duncan,The Transformations [or Metamorphoses] of Insects [Philadelphia: Claxton, Remsen, and Haffelfinger, 1870], p. 338); “Mr. Charles O. Waterhouse sent for exhibition a living specimen of a Mantid... The captor stated that he had supplied it with flies, &c., in the hope of ascertaining the mode in which it seized them” (Edward Newman, ed., “A Living Mantid Exhibited,”Entomologist, 7 [1874], 188); “... our fastidious captive had his meals servedau naturel. The living fly was simply turned loose in his cage, and instantly the devil's-riding-horse was on alert” (Bellamy, “Queer Pet” [above, n. 46], p. 530); “The food of this tribe of insects [i.e., mantids] being flies of any kind” (Mrs. Brighton,Inmates of My House and Garden [New York: Macmillan, 1895], p. 204); “This is the way the house-flies rightfully take the mantis's attitude. Watch an unwary bluebottle crawl or buzz into the fatal corner” (Vernon J. Kellogg,American Insects [New York: Henry Holt, 1905], p. 129); “[Trimen] also describes its mode of feeding, and says that it was fond of house-flies, and would eat ‘blue-bottles,’ i.e.,Musca vomitoria” (S. F. Harmer and A. E. Shipley, eds.,The Cambridge Natural History, vol. V [London: Macmillan, 1922], p. 274). As we will explain, the belief that mantid predation is limited to fly-sized insects would eventually come to play a critical role in shaping both experimental paradigms using the mantis, and interpretations of the results derived from those experiments.

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  55. (Again note the reliance on flies as the primary food for the captive mantis.) H. C. C. Burmeister, “Kaukerfe.Gymnognatha. Ersta Hälfe;vulgo Orthoptera,” inHandbuch der Entomologie (Berlin, 1838), pp. 397–756; cited in Kevan, “The Mantis and the Serpent,” (above, n. 26), p. 3. These early accounts were cited in many popular books (e.g., A. S. Packard,Guide to the Study of Insects [Salem: Naturalist's Book Agency; and London: Trübner, 1869], p. 575;Cambridge Natural History, V, 250), and articles on mantids (e.g., “Mantidae,”Sci. Amer., 66 [1892], 375). Most of the literature on mantid predation on vertebrates is reviewed in Kevan's article, but also see John S. Kingsley, ed.,The Standard Natural History (Boston: S. E. Cassino, 1884), p. 176; M. D. Johnson, “Concerning the Feeding Habits of the Praying Mantis,Tenodera aridifolia sinensis, Saussure,”J. Kans. Entomol. Soc., 49 (1976), 164; M. G. Ridpath, “Predation of Frogs and Small Birds byHerodula Werneri, Mantidae in Tropical Australia,”J. Austral. Entomol. Soc., 16 (1977), 153–154; D. A. Nickle, “Predation on a Mouse by the Chinese MantidTenodera aridifolia sinensis, Saussure (Dictyoptera: Mantoidea),”Proc. Entomol. Soc. Wash., 83 (1981), 802–803.

  56. W. F. Erichson, ed., “Zur Naturgeschichte derMantis Carolina: aus einem Schreiben des Dr. Zimmermann,”Arch. Naturgesch., 9 (1843), 390–392; cited in Kevan, “The Mantis and the Serpent” (above, n. 26), p. 3.

  57. AlfredTulk, “Habits of the Mantis”Ann. Mag. Nat. Hist., 14 (1844), 78.

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  58. J. H.Fabre,Souvenirs entomologiques, 10 vols. (Paris: Librairie Ch. Delagrave, 1879–1907). The praying mantids are discussed in vol. V, pp. 287–355. The work was translated into English by A. Teixiera de Mattos asThe Works of J. Henri Fabre (London, 1912). In addition, various popular condensations of Fabre's work were published, such as Mrs. Rodolph Stawell,Fabre's Book of Insects (New York: Tudor, 1921 and 1936), and Edwin Way Teale,The Insect World of J. Henri Fabre (New York: Dodd, Mead, 1949).

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  59. “These particular captures are destined to show me just how far the vigor and audacity of the Mantis will lead it. They include the large grey cricket... which is larger than the creature that devours it” (J. H.Fabre [Bernard Miall, trans.],Social Life in the Insect World [London and Leipzig T. Fisher Unwin, 1912] p. 73). Similar anecdotal accounts of the mantid's catholic tastes appeared in the early twentieth-century entomological literature. For instance: “Full grown adults if hungry ate almost any living thing... [even] huge cockroaches and grasshoppers as large as themselves” (Mary Didlake, “Observations on Life-Histories of Two Species of Praying Mantis [Orthopt.: Mantidae],”Entomol. News, 37 [1926], 170).

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  60. J. H.Fabre [Bernard Miall, trans.],Social Life in the Insect World [London and Leipzig: T. Fisher Unwin, 1912], pp. 74–75. “With the smaller crickets... the Mantis rarely employs her means of intimidation; she merely seizes the heedless passerby as she lies in wait” (ibid, p. 76).

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  61. This is the only instance of which we are aware that mantid cannibalism is linked to a mantid's gender. Fabre's observations, that adult females are more likely to eat conspecifics than are adult males, are supported by other observations; for instance “... never yet have I seen an adult male attack either a female or another of its own sex” (PhilRau and NellieRau, “The Biology ofStagmomantis Carolina”Trans. Acad. Sci. St. Louis, 22 [1913], 19). The reason for the difference in behaviors is that adult females are usually larger and stronger, and eat more than adult males. However, we have seen maleSphodromantis lineola, (Burr.) eat male conspecifics.

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  62. (J. H.Fabre [Bernard Miall, trans.]),Social Life in the Insect World [London and Leipzig: T. Fisher Unwin, 1912, p. 81.

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  63. (J. H.Fabre [Bernard Miall, trans.]),Social Life in the Insect World [London and Leipzig: T. Fisher Unwin, 1912, p. 84. Similarly, the well-known Swedish entomologist Charles de Geer (1720–78) reported being filled with “horror and indignation” at the sight of a male spider being captured and eaten “in the midst of his preparatory caresses” (Charles de Geer,Mémoires pour servir à l'histoire des insectes [Stockholm: 1758], VII, 335; cited in Kirby and Spence,Introduction to Entomology [above, n. 48], I, 272).

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  64. J. H.Fabre [Bernard Miall, trans.],Social Life in the Insect World [London and Leipzig: T. Fisher Unwin, 1912, pp. 84–85.

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  65. This analogy is borrowed from the following articles, to which the reader should turn for a thorough experimental analysis of courtship behavior in one species of mantid: E.Liske and W. J.Davis, “Sexual Behavior of the Chinese Praying Mantis,”Anim. Behav., 32 (1984), 916–917; E. Liske and W. J. Davis, “Courtship and Mating Behavior of the Chinese Praying Mantis,Tenodera aridifolia sinensis,” Anim, Behav., 35 (1987), 1524–37.

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  66. R. F.Chapman,The Insects (Cambridge, Mass. Harvard University Press, 1982), pp. 607–641; Cedric Gillott,Entomology (New York: Plenum, 1980), pp. 361–420.

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  67. E. M.Einstein amd M. J.Cohen, “Learning in an Isolated Prothoracic Insect Ganglion,”Anim. Behav., 13 (1965), 104–108.

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  68. Poiret's observation, published originally inJournal de Physique in 1784, is cited in L. F.Henneguy,Les insectes (Paris: Masson, 1904), p. 263. In turn, this reference is cited in Étienne Rabaud, “Accouplement d'un mâle décapité deMantis religiosa, L. (Orth.),”Bull. Soc. Entomol., 21 (1916), 57. The other two articles are Raphel Dubois, “Sur l'innervation réflexe chez la mante religieuse,”Prés. Soc. Linn. Lyon, 40 (1893), 205–207 (in which an article by Duges appearing in the same volume of the journal is cited); and L. Chopard, “Sur la vitalité deMantis religiosa, L. (Orth. Mantidae); ponte après décapitation,”Bull. Soc. Entomol. Fr., 19 (1914), 481–482. It is noteworthy that Chopard cited the Dubois article, and Rabaud cited both Dubois and Chopard. Although, to the best of our knowledge, these articles were never published in English, they were well known and frequently cited in scientific and popular literature, as will be explained. Translations of these articles from French into English have been done especially for this paper by Ms. Cathryn Easterbrook.

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  69. Dubois, “Sur l'innervation réflexe,” pp. 205, 206. One reads a similar item in N. Hudson Moore, “The Mantis Religiosa in Rochester, N.Y.,”Sci. Amer., 84 1901, 105–106: “The loss of head, or a leg or two, or even a portion of the body does not quench the fiery nature of a fighting Mantid, but they may go on battling in this condition for hours” (p. 106).

  70. Chopard, “Sur la vitalité deMantis religiosa,” pp. 481–482.

  71. ÉtienneRabaud, “Accouplement d'un mâle décapité deMantis religiosa, L. (Orth.),”Bull. Soc. Entomol., 21 (1916), pp. 57–59.

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  72. Brown, “Of Mantises and Myths,” (above, n. 10), p. 421. Also note, for instance, “[Howard's article] represents the first account I know of an all-time favorite among nature's curious facts” (Gould, “Only His Wings Remained” [above, n. 9], p. 10).

  73. “Westwood quoted from theJournal de Physique, 1784, an instance in which the female of the European species ... decapitated the male before mating... Riley in his ‘First Monthly report,’ p. 151. wrote, ‘The female being the strongest and most voracious, the male in making his advances, has to risk his life many times, and only succeeds in grasping her by slyly and suddenly surprising her; and even then he frequently gets remorselessly devoured,’ In Packard's ‘Guide,’ p. 575, we find, “Professor Sandborn Tenny tells me he has observed the female after sexual union devour the male” (Howard, “Excessive Voracity” [above, n. 8], p. 326).

  74. Ibid.

  75. C.Riley and L.Howard, “The Female Rear-Horse versus the Male,”Insect Life, 5 (1892), 145. This article was translated into Swedish as S. Lampa, “Engendomliga vanir hos Mantidernas honor,”Entomol. Tidskr., 15 (1894), 118. It should also be noted that another account of a femaleS. carolina devouring a malein copulo appeared shortly thereafter in W. S. Baltchley, “Miscellaneous Notes,”Can. Entomoll. 28 (1896), 210–215.

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  76. If male-on-female cannibalism occurred with any frequency, we are sure that a story would have sprung up claiming that the female has evolved such that decapitation releases the egg-laying response from cerebral inhibition (recall Chopard's account).

  77. B.Aoki and S.Takeishi “On the Copulatory Behavior of the Japanese Mantis (Tenodera aridifolia, Stoll.), and the Seat of Its Nerve Center,”Dobutsugaku Zasshi, 39 (1927), 114–129. The authors demonstrated that that males will copulate when their heads are “killed” or severed, and (as Chopard indicated) that females will continue to lay egg cases after decapitation. The authors concluded that “this peculiarity [on the part of the males] is adaptive ... in view of the fact that the male is often eaten up by the female while approaching its mate or even during copulation” (p. 128). In support of the latter contention, the authors included two photographs of several headless males mating. Ironically, the captions read “Naturel copulation” (p. 127, italics added). It is of note that no evolutionary significance is attached to the decapitated female's egg-laying abilities.

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  78. Rau and Rau, “Biology ofStagmomantis carolina” (above, n. 62), p. 29 (italics added).

  79. Ibid., p. 39.

  80. Ibid., plate III. The Raus had read Riley and Howard's work, including the pertinent article.

  81. H. MaxwellLefroy,Manual of Entomology (New York: Longmans, Green; and London: Edward Arnold, 1923), p. 49.

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  82. William MorrisWheeler,Foibles of Insects and Men (New York: Knopf, 1928), p. 160.

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  83. Edwin WayTeale, “Dinosaur of the Insect World,”Travel, 64: 4 (1935), 25.

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  84. K. D.Roeder, “An Experimental Analysis of the Sexual Behavior of the Praying Mantis (Mantis religiosa, L.)”Biol. Bull., 69 (1935), 203–220. Roeder's findings were also explained in his popularNerve Cells and Insect Behavior (Cambridge, Mass.: Harvard University Press, 1963), pp. 129–170.

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  85. Roeder cited M. Morgue, “Un reptile chassé et tué par un insecte,”Feuille Jeunes Nat., (1909), 87.

  86. Roeder, “Experimental Analysis,” p. 205.

  87. Also see K. D.Roeder, “The Control of Tonus and Locomotor Activity in the Praying Mantis (Mantis religiosa, L.),”J. Exp. Zool., 76 (1937), 353–374.

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  88. In addition, Roeder found that removal of the SEG yields a general drop in muscle tone, spontaneous locomotor movements (occurring simultaneously with the copulatory movements), and immediate, grasping of any rounded object accompanied by “violent attempts” at copulation (“Experimental Analysis,” pp. 212–213).

  89. This was indicated to Roeder by the fact that when “the nerve cord in the abdomen is... cut at various levels, the movements of the cerci and claspers continue while [only] the last abdominal ganglion is intact” (ibid., p. 216). The idea that complex behaviors were organized within individual ganglia was already an accepted belief among entomologists. See, for instance, E.Baldi, “Studi sulla fisiologia del sistema nervoso negli insetti,”J. Exp. Zool., 36 (1922), 211–288; A. Bethe, “Nervous System of Arthropods,”J. Comp. Neur., 8 (1898), 232–238; W. von Buddenbrock, “Rythmus des Schreitbewegungen der Stabheuschrecke,Dixippus morosus,” Biol. Zentralbl., 41 (1921), 41–48; H. Z. Ewing, “The Functions of the Nervous System with Special Regard to Respiration in Acrididae”,Univ. Kans. Sci. Bull. 2 (1904), 305–319; S. Kopec, “Über die Funktionen des Nervensystems der Schmitterlinge während sukzessiven Stadien ihrer Metamorphose,”Zool. Anz., 40 (1912), 353–360.

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  90. K. D.Roeder, “An Experimental Analysis of the Sexual Behavior of the Praying Mantis (Mantis religiosa, L.)”Biol. Bull., 69 (1935), pp. 217–218.

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  91. “Insects up to the size of the mantis may be caught and eaten, including other mantids of the same species. This fortuitous cannibalism is probably minimized in nature by the inactive and cryptic habits of mantids.... [A] cannibalistic attack may take place during the male's [courtship] approach, directly after mounting, or as the couple separates... It is not inevitable, and appears to depend upon the female's state of nutrition, and upon her detection of the male's movements during the final phase of his approach” (Roeder,Nerve Cells [above, n. 85], pp. 132–134; and see Roeder, “Experimental Analysis,” pp. 204–209).

  92. Roeder,Nerve Cells, p. 136. Again, note the inconsistency in Roeder's claims. The statement cited is much stronger than that made in the conclusion of the original paper: “When the male is attacked by the female he is usually seized by the raptorial arms or the head, and these are devoured first” (“Experimental Analysis,” p. 218). However, Roeder makes an equally strong claim in the summary section of the same paper: “Since the headis attacked first ...” (“Experimental Analysis,” p. 219; italics added).

  93. Roeder, “Experimental Analysis,” p. 218.

  94. As an example of the extent to which the belief in the inevitability of mating-related cannibalism remained embedded in the literature, consider the report on mating in the Trinidad mantis,Acontiothespis multicolor, published in 1967. Although the author found no instances of mating-related cannibalism in this species, he stated that his orginal purpose was “to see whether or not the female habitually devours the male after mating as is apparently the case with the European mantis” (V. C. Quesnel, “Observations on the Reproductive Behavior of the Mantis,Acontiothespis multicolor,” Trinidad Field Nat. Club., [1967], 53).

  95. PeterMarler and WilliamHamilton,Mechanisms of Animal Behavior (New York: Wiley, 1967), pp. 208–210.

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  96. Darryl T.Gwynne, “Male Nutritional Investment and the Evolution of Sexual Differences in Tettigoniidae and Other Orthoptera,” inOrthopteran Mating Systems, ed. Darryl T.Gwynne and Glenn K.Morris (Boulder, Col.: Westview Press, 1983), p. 346.

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  97. J. L.Gould,Ethology (New York: W. W. Norton, 1982), p. 365. Also note: “Females commonly attack and devour males either before or after copulation. ... Destruction of the [subesophogeal] ganglion allows copulation to proceed” (Vernon Vickery and D. Keith McE. Kevan,The Insects and Arachnids of Canada [Canada: Agriculture Canada, 1985], p. 89).

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  98. As we have noted, the earliest accounts of cannibalism refer only to mantid pugnaciousness, not to gender. Nor did gender enter into subsequent, popular accounts of mantid cannibalism. Characteristic is this description: “If two of these insects be shut up together ... they deal each other blows with their front legs, and do not leave off fighting until the stronger has succeeded in eating off the other's head” (“The Mantis or Praying Insect,”Pop. Sci. Mon., 4 [1874], 711). Virtually the same account appears in Figuier,Insect World (above, n. 55), p. 290; the latter account simply adds as a matter of fact that “The male being smaller than the female, is often its victim.” In fact, voraciousness was attributed equally to both sexes: “The winner, that is to say the survivor, generally consummates his victory by devouring the body of his slaughtered foe” (J. G. Wood,The Illustrated Natural History [London: Routledge, 1871], p. 485).

  99. See, e.g., JohnRay,Historia insectorum (London: A. & J. Churchill, 1710).

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  100. In addition to those texts already mentioned, see: DruDury,Illustrations of Natural History, vol. I–III (London: B. White, 1770–82), in which species of mantids from Jamaca, India, and America are described in each volume; Hans Sloane,A Voyage to the Islands ... and Jamaca, vol. II (London: for the author, 1725); and George Shaw,Naturalist's Miscellany (London: Nodder, 1789–1813).

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  101. Anthony A. H.Lichtenstein (translated from the German by Thomas Young), “A Dissertation on Two Natural Genera Hitherto Confounded under the Name of Mantis,”Trans. Linn. Soc., 6 (1802), 1–39. As Lichtenstein noted (p. 2), his argument had been mounted earlier by Casper Stoll inNatuurlyke, en naar't leeven nauwkeurig gekleurde Afbeeldingen, en Beschryyingen der Spooken, Wandelnde Bladen, Zabelspringhanen, Krekels, Trekspringhaanen en Kakkerlakken (Amsterdam: J. C. Sepp, 1797), the publication of which was interrupted by the author's death.

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  102. Note this example of the charm of the human-like qualities of the mantis's gaze: “A dignitary of the Natal Church ... was, one warm summer evening ... preaching by candle light ... when a huge green mantis ... perched himself upon the preacher's white neckerchief ... first folding his arms into the prayerful attitude, he raised his chest and shoulders into rapt attention, turning his goggles from side to side, and following responsively. ... He remained fixed in this convenient position until properly dismissed with the rest of the congregation” (an account by a Dr. Mann, cited in “The Mantis of Praying Insect” [above, n. 99], p. 713). Also note the comment that “[the mantis] is the only insect which appears to see man as an individual” Lefroy,Manual of Entomology [above, n. 82], p. 48.

  103. The fully articulated head and neck are unique among the insects. Of note also is the fact that as the observer moves in relation to the insect's head, the mantis appears to be following the observer with its gaze: “These animals have a small black pupil or sight, which moves in all directions within the parts that we usually term eyes” (T. Smith,Naturalist's Cabinet [above, n. 47], VI, 290). The reason for the illusion has to do with the construction of the insect's compound eyes. The compound eye is made up of individual ommatidia or columns of cells each capped with a lens. Together the lenses form the mosaic of facets covering the convex outer surface of the eye. From any given position, then, one is looking directly into one or several ommatidia, which (because no light is reflected back out) appear as a black spot, similar to the pupil in a person's eye. As one moves in relation to the insect's eye, the pseudopupil moves too, giving the impression that the mantid is following with its gaze. This, in conjunction with the mantid's almost human-like head movements (which may, indeed, follow the passer by), make the mantid's gaze quite captivating.

  104. Lichtenstein, “Dissertation,” p. 7. Earlier, Lichtenstein described the raptorial forelegs as “falciform hands, and a thumb” (p. 4).

  105. Anthony A. H.Lichtenstein (translated from the German by Thomas Young), “A Dissertation on Two Natural Genera Hitherto Confounded under the Name of Mantis,”Trans. Linn. Soc., 6 (1802), 4–5.

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  106. “Notes from the Zoo — The Praying Mantis,”Saturday Rev., 69 (1890), 735; Harold Bateson,Insects Their Life-Histories and Habits (London: T. C. and E. C. Jack, 1913), p. 174. This idea was carried to its logical extreme in several accounts that suggested that the forelegs were so highly adapted for predation that they could no longer be used for locomotion! See “Mantidae,”Sci. Amer., 66 [1892], 375; Bateson,Insects, p. 63; Harmer and Shipley,Cambridge Natural History (above, n. 55), p. 251.

  107. In addition to the references already cited, see O. W.Richards, “Sexual Selection and Allied Problems in the Insects,”Biol. Rev., 2 (1927), 331.

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  108. Ethology, with its roots in central European biology, is best known through the works of Konrad Lorenz, Niko Tinbergen, and Karl von Frisch, who were jointly awarded the Nobel Prize for physiology or medicine in 1973. Of these three, Lorenz was the key figure in establishing the discipline of ethology in continental Europe. For a general account see W. H.Thorpe,The Origins and Rise of Ethology (London: Heinemann, 1979).

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  109. See, e.g., Jacob von Uexküll,Umvelt und Innenwelt (Berlin, 1909); Konrad Lorenz, “The Comparative Method in Studying Innate Behavior Patterns,”Symp. Soc. Exp. Biol., 4 (1950), 421–468; idem,The Foundations of Ethology (New York: Springer-Verlag, 1981); and Niko Tinbergen,The Study of Instinct (Oxford: Oxford University Press, 1951).

  110. See NorbertWiener,Cybernetics (Cambridge, Mass.: MIT Press, 1948). Also see Graham Hoyle, “The Scope of Neuroethology,”Behav. Brain Sci., 7 (1984), 368.

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  111. In 1950 von Holst invited a group of the Continent's outstanding ethologists to his Max Plank Institut für Verhaltensphysiologie (founded at Seewiesen) for an informal ten-day conference. The group included Konrad Lorenz, Otto Koehler, Gustav Kramer, Wolfgang Metzger, Ursula von Saint Paul, Laura Schoen, Niko Tinbergen, William Thorpe, and two of von Holst's students, Bernard Hassenstein and Horst Mittelstaedt. The meetings of this group of scientists were the forerunners of the long-standing, biannual International Ethological Conferences (Thorpe,Origins and Rise of Ethology, pp. 82–84).

  112. For an overview, see HorstMittelstaedt: “Prey Capture in Mantids,” inRecent Advances in Invertebrate Physiology, ed. B. T.Scheer (Eugene: University of Oregon Publications, 1957), pp. 51–71; and “Control Systems of Orientation in Insects,”Ann. Rev. Entomol., 7 (1962), 177–198. Although Konrad Lorenz worked with vertebrates, Tinbergen and Berends did important work on insects, and von Holst and his students were particularly interested in the endogenous generation of motor patterns in invertebrates, including insects. The suggestion has been made that the attraction of invertebrates for many early ethologists lay in the putative simplicity of these animals (as compared to vertebrates), giving the impression that their central nervous systems are more “transparent” and are amenable to analysis via behavioral experimentation (Dr. Richard Burkhart, University of Illionis, Champaign-Urbana, pers. comm.).

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  113. See, for example, in Europe: P.Lässig and K.Krimse, “Optimotor Tracking Movements of Mantis Religiosa,” inBiocybernetics, ed. H.Drischel and P.Dettmar (Jena: Gustav Fischer, 1971), IV, 242–246; E. Liske, “Proprioceptive Control of Head Position and Head Movement in the Praying Mantis,”Naturwissenschaften, 69 (1982), 452–453; E. Liske and W. Mohren, “Saccadic Head Movements of the Praying Mantis, with Particular Reference to Visual and Proprioceptive Information,”Physiol. Entomol., 9 (1984), 29–38. In the United States; J. Y. Lea and C. G. Mueller, “Saccadic Head Movements in Mantids,”J. Comp. Physiol., 114 (1977), 115–128; Susan Rilling, H. Mittelstaedt, and K. D. Roeder, “Prey Recognition in the Praying Mantis,”Behav., 14 (1959), 164–184. In South America: H. Maldonado and J. C. Barros-Pita, “A Fovea in the Praying Mantis Eye. I. Estimation of the Catching Distance,”Z. vergl. Physiol., 67 (1970), 58–78; H. Maldonado, M. Benko, and M. Isern, “A Study of the Role of the Binocular Vision in Mantids to Estimate Long Distances, Using the Deimatic Reaction as Experimental Situation,”Z. verg. Physiol., 68 (1970), 72–83; H. Maldonado, L. Levin, and J. C. Barros-Pita, “Hit Distance and the Predatory Strike of the Praying Mantis,”Z. vergl. Physiol., 56 (1967), 237–257.

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  114. This misunderstanding seems to have happened for several reasons. The first is the basic assumption that mantid behavior can be adequately described as a hierarchy of simple reflexes. The second is the somewhat limited explanatory power of control theory itself, which does not (nor does it pretend to) mirror the actual biological units that make up the organism. Third, by the time that control theory gave way to newer models that recast animal behavior as more variable, plastic, and context dependent, mantid behavior had already been (it seemed) pretty thoroughly described, and the insect was seldom used in behavioral studies. Finally, experimental paradigms using a tethered, inverted mantis (and a more recent variant involving an inverted mantid restricted to a small platform) constrain the mantid's prey-catching behaviors, thereby giving the impression that the behaviors are more limited than they really are. For a comparison of the behavior of freely moving versus movement-restricted mantids of one species, see F. R.Prete, C. A.Klimek, and S. P.Grossman, “The Predatory Strike of the Praying Mantis,Tenodera aridifolia sinensis,”J. Insect Physiol., 36 (1990), 561–565.

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  115. Rilling, Mittelstaedt, and Roeder, “Prey Recognition.”

  116. It is of great interest that, as usual, the investigators maintained their mantids on a diet of flies.

  117. This rarely cited study found thatHierodula crassa, (G.-Tos.) responds most strongly to a 8×24 mm (1.92 cm2) lure rotating around its long axis (C. S.Holling, “The Analysis of Complex Population Processes,”Can. Entomol., 96 [1964], 335–347). It has recently been demonstrated that one species of mantis responds with predatory behaviors both to compact lures (such as those used by Rilling) and to large lures which are elongated parallel to their direction of movement (such as those used by Holling). This pattern of responding is similar to that seen in other terrestrial predators, such as toads (e.g.,Bufo bufo) (F. R. Prete, “Configural Prey Recognition by the Praying Mantis,Sphodromantis lineola, [Burr.]; Effects of Size and Direction of Movement,”Bran Behav. Evol., 36 [1990], 300–306).

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  118. In addition to studies previously mentioned, see C. S.Holling, “The Functional Response of Invertebrate Predators to Prey Density,”Mem. Entomol. Soc. Can., 48 (1966), 3–47; and R. G. Loxton and I. Nicholls, “The Functional Morphology of the Praying Mantis Forelimb (Dictyoptera: Mantodea),”Zool. J. Linn. Soc., 66 (1979), 185–203. Note also the assumption that the mantis's visual system is specifically evolved to locate prey of “typical size” (read: “flysized”) in S. Rossel, “Foveal Fixation and Tracking in the Praying Mantis,” and “Binocular Spacial Localization in the Praying Mantis,”J. Exp. Biol., 120 (1986), 265–281. And note the exclusive use of flies as lures, and the assumption that the mantis's eyes have evolved to best localize flies when they are at the “optimum” catching distance in the following three studies: H. Maldonado and J. C. Barros-Pita, J. C. Barros-Pita and H. Maldonado, and L. Levin and H. Maldonado, “A Fovea in the Praying Mantis Eye,” Parts 1, 2, and 3,Z. vergl. Physiol., 67 (1970), 58–78, 79–92, and 93–101.

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  1. Department of Psychology, Youngstown State University, 44555, Youngstown, Ohio, USA

    Frederick R. Prete & M. Melissa Wolfe

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Prete, F.R., Wolfe, M.M. Religious supplicant, seductive cannibal, or reflex machine? In search of the praying mantis. J Hist Biol 25, 91–136 (1992). https://doi.org/10.1007/BF01947506

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