Parasite Rex: Inside the Bizarre World of Nature's Most Dangerous Creatures

Notes

Prologue: A Vein Is a River

xiv “Trypanosoma brucei has many enchanting features …”: Borst et al., 1997, p. 121.

xvi Over 1.4 billion people carry the snakelike roundworm: These statistics come from Crompton, 1999.

1. Nature’s Criminals

1 “Nature is not without a parallel …”: Brown, 1898.

2 Eventually the parasite became a standard character: Damon, 1997.

2 Aristotle, for instance, recognized creatures: Grove, 1990.

2 two serpents wound around a staff: Roberts and Janovy, 2000.

3 “The substance in question cannot be a worm …”: Quoted in Grove, 1990, p. 121.

4 “Some shoot forth horns …”: Quoted in Wilson, 1995, p. 160.

5 The mysterious nature of parasites: See Farley, 1972.

6 “arches over them like a small, closely shut watch glass.”: Quoted from Steenstrup 1845, pp. 57–58.

7 “An animal bears young …”: Quoted from Steenstrup, 1845, p. 132.

8 “It would be contrary to the wise arrangement of Nature …”: Quoted in Farley, 1972, p.120. For more details on the discovery of tapeworm life cycles, see also Grove, 1990, and Foster, 1965.

11 By 1900, bacteria were rarely called parasites anymore: Worboys, 1996.

11 When Leeuwenhoek had looked at his own feces: Roberts and Janovy, 2000.

13 When Napoleon took his army to Egypt: Nelson, 1990.

14 in the words of one scientist at the time, “medical zoology.”: Worboys, 1983.

14 “It is derogatory that the Creator …”: Quoted in Desmond and Moore, 1991, p. 293.

15 “I cannot persuade myself that a beneficent and omnipotent God …”: Quoted in Desmond and Moore, 1991, p. 479.

15 To their mind, orthogenesis brought a purpose: Bowler, 1983.

15 One influential voice for orthogenesis: Lester, 1995.

16 “the jack-in-office, the pompous official …”: Quoted in Lester, 1995, p. 59.

16 For biologists of Lankester’s day: Cox, 1994.

17 “Let the parasitic life once be secured …”: Lankester, 1890, p. 27.

17 Drummond declared that parasitism “is one of the gravest crimes …”: Quoted from Drummond, 1883, p. 319.

18 “All those indiviudals who have secured a hasty wealth …”: Quoted from Drummond, 1883, p. 350.

18 “In the struggle for daily bread …”: Quoted from Hitler, 1971, p. 285.

18 “only and always a parasite in the body of other peoples.…”: Quoted from Hitler, 1971, p. 304.

19 To Marx and Lenin: See Brennan, 1995.

19 “With the refinement of innate cruelty …”: Quoted from Brown, 1898, pp. 162–163.

19 “Freedom, bondage, and the welfare state”: Stunkard, 1955.

21 “When we use the terms ‘higher and lower’ …”: Quoted from Lorenz, 1989, p. 41.

22 “A retrogression of specific human characteristics …”: Lorenz, 1989, p. 45.

22 “I believe that I have given …”: Quoted from Steenstrup, 1845, p. 8.

2. Terra Incognita

24 Consider the blood fluke Schistosoma mansoni: This description is drawn mainly from Basch, 1991.

27 This tiny nematode comes our way: Campbell, 1983.

29 Sukhdeo ignored the advice: Sukhdeo summarizes his work in Sukhdeo, 1997.

31 In tropical countries, between 30 and 90 percent of cattle carry them: Spithill and Dalton, 1998.

36 Each of these copepods looks so different: For an overview of parasitic copepods, see Benz, in preparation.

36 As they feed, tapeworms grow at a spectacular rate: Roberts and Janovy, 2000.

37 When we eat, peristalsis immediately ripples through our intestines: See Sukhdeo, 1997.

37 The intestines are also home to hookworms: See Hotez et al., 1995; Hotez and Prichard, 1995.

38 A biotechnology company has isolated these molecules: For information on the company’s work, see its web site: www.corvas.com.

40 To do so, they set down hooks on the vessel wall: Naitza et al., 1998.

41 Fifteen seconds after the blast: Only one species of Plasmodium invades red blood cells this way: P. falciparum, which causes the most dangerous kind of malaria.

41 The core of hemoglobin: Ginsburg et al., 1999.

42 In other words, Plasmodium has to transform these mere corpuscles: This description of how Plasmodium invades and rebuilds blood cells is drawn from Foley and Tilley, 1995, 1998; Sinden 1985.

42 In either case, the parasitized red blood cell can start dragging: Lauer et al., 1997.

43 Trichinella is also a biological renovator: See Capo et al., 1998; Despommier, 1990; Polvere et al., 1997.

44 Plants are even hosts to parasitic plants: See Press and Graves, 1995; Stewart and Press, 1990.

45 But many plant-eating insects spend: Thompson, 1994.

45 nematodes that live in plant roots: For reviews of root nematodes, see Bird, 1996; Niebel, et al.; 1994.

47 Bigger hosts tend to have more species of parasites in them: Poulin, 1995.

47 On the gills of a single fish: Rhode, 1994. For other examples of parasite niches, see Roberts and Janovy, 2000; Kennedy and Guegan, 1996.

47 When parasitologists crack open the shells of snails: Kuris and Lafferty, 1994.

48 The wasp Copidosoma floridanum: Strand and Grbic, 1997.

50 The adult filarial worms live in the lymph channels: Roberts and Janovy, 2000.

50 The fleas on a female rabbit’s skin: Hart, 1994.

51 Dig a few feet down into the hard summer dirt: For details of Pseudodiplorchis, see Tinsley, 1990; Tinsley, 1995, and the references therein.

3. The Thirty Years’ War

55 A man came one day to the Royal Perth Hospital: Harris et al., 1984.

57 But here, at any rate, is a brief survey: Janeway and Travers, 1994.

60 In September 1909, a strong young man: Ross and Thomson, 1910.

62 “a struggle between the defensive powers of the infected body …”: Quoted from Ross and Thomson, 1910, p. 408.

62 They play an exhausting game of bait-and-switch: See Barry, 1997; Borst et al., 1997.

64 Because these latches can be recognized by the immune system: Borst et al., 1995.

65 Each species causes a disease of its own: Bloom, 1979.

65 Leishmania doesn’t have to muscle its way: For details of Leishmania’s invasion, see Bogdan and Rollinghoff, 1999; Locksley and Reiner, 1995.

67 Few people know about Toxoplasma: For Toxoplasma’s evasions, see Sher, 1995.

70 One remarkable example is the tapeworm: White et al., 1997.

72 You can see their disguise at work in a simple experiment: Damian, 1987.

73 a paradox on the shores of Lake Victoria: Karanja et al., 1997.

74 Under the spell of the eggs: Leptak and McKerrow, 1997.

76 The parasite survives thanks to millions of viruses: For reviews of Cotesia congregata and its viruses, see Beckage, 1997, 1998; Dushay and Beckage, 1993; Lavine and Beckage, 1996.

4. A Precise Horror

79 biologists of his day just didn’t know much: My description of Sacculina is drawn from Collis and Walker, 1994; DeVries et al., 1989; Gilbert et al., 1997; Glenner and Høeg, 1995; Glenner et al., 1989; Glenner et al., 2000; Hartnoll, 1967; Høeg, 1985a, 1985b, 1987, 1992, 1995; Lutzen and Høeg, 1995; O’Brien and Van Wyk, 1986; O’Brien and Skinner, 1990; Raibaut and Trilles, 1993.

82 This puppetry takes different forms: For general reviews of host manipulation, see Moore, 1995; Moore and Gotelli, 1996; Poulin, 1994.

82 Rather than just passively soak up the food: Thompson, 1993.

83 A fungus called Puccinia: Roy, 1993.

84 The wasps seem to be responsible for the anorexia: Adamo, 1998.

84 Another species of wasp goes even further: Brodeur and Vet, 1994.

84 There are parasitic nematodes: Vance, 1996.

86 A fungus that lives inside house flies: Krasnoff et al., 1995.

87 Along the coasts of Delaware lives a fluke: Curtis, 1987, 1990.

87 Known as Dicrocoelium dendriticum: Roberts and Janovy, 2000.

88 The guinea worm spends its early life: Roberts and Janovy, 2000.

90 When a mosquito lands on your arm: For the challenges mosquitoes face, and the way Plasmodium manipulates them, see Day and Edman, 1983; James and Rossignol, 1991; Koella, 1999; Koella et al., 1998b; Ribeiro, 1995.

90 A mosquito with ookinetes in it: Anderson et al., 1999.

91 A fluke called Leucochloridium: Roberts and Janovy, 2000.

91 Some species of tapeworms live in the guts of: LoBue and Bell, 1993.

91 They can also alter the behavior: Tierney et al., 1993.

92 A small crustacean named: Helluy and Holmes, 1989.

92 Toxoplasma, the protozoan lodged: Berdoy et al., 2000.

95 Moore built chambers out of Pyrex pie plates: Moore, 1983.

97 Their hunger pushes the sticklebacks to take more risks: Milinski, 1990.

97 Biologists have pulled out the neurons of Gammarus: Helluy and Holmes, 1989; Maynard et al., 1996.

99 Beetles are lured to egg-bearing droppings: Evans et al., 1992.

99 If you trap the fragrance of infected dung: Evans et al., 1998.

99 the tapeworm then uses more chemicals: Hurd, 1998; Webb and Hurd, 1999.

100 Put it on a pile of flour: Robb and Reid, 1996.

100 But once the tapeworm reaches maturity: Blankespoor et al., 1997.

104 oceans are swarming with viruses: Fuhrman, 1999.

104 For decades, ecologists who worked on the Serengeti: Dobson, 1995.

106 In fact, if you were to get rid of the fluke: Lafferty, 1993a.

108 The results were even more stark: Lafferty describes his experiments in Lafferty, 1997a; Lafferty and Morris, 1996.

109 But why would birds: Lafferty models the trade-offs for hosts like these birds in Lafferty, 1992.

109 ecologist Greta Aeby has been scuba diving: Aeby, 1992, 1998.

111 they’ve contained fifteen quarts of fluid: Roberts and Janovy, 2000.

111 The thinning of the herd is an illusion: Messier et al., 1989; Rau and Caron, 1979.

115 It makes the corpse of its host a sexual magnet: Møller, 1993.

115 “I wonder why the titans …”: Quoted from Heinlein, 1990, p. 205.

116 delusional parasitosis: Wykoff, 1987.

5. The Great Step Inward

122 The closest match he found: For the discovery of the apicoplast and its relationship with chloroplasts, see Kohler et al., 1997, and the references therein.

125 the eukaryotes with their DNA: Some of the most primitive eukaryotes such as Giardia are missing mitochondria, but recent gene sequencing has suggested that they originally had the organelle and lost it later in their evolution. (See, for instance, Hashimoto et al., 1998.) These results point to the first eukaryotes as having mitochondria.

125 the dawn of the age of eukaryotes: Knoll and Carroll, 1999.

126 Parasitism is any arrangement: Dawkins, 1982.

127 genetic parasites: Sherratt, 1995.

127 Some of them steal genes from their host: Xiong and Eickbush, 1990.

127 How is it, for instance, that a freshwater: Robertson, 1997.

128 Eventually the coalition of genes got organized: For this promiscuous vision of the beginning of life, see Woese, 1998.

128 It was probably at this time that life began to diverge: Katz, 1998.

129 If the cost of trying to fight off the invasion: Law, 1998.

129 But biologists now recognize: Doolittle, 2000.

129 Among the fully sequenced species is Rickettsia: Muller and Martin, 1999.

130 This billion-year-old drama: Roos et al., 1999.

131 David Roos and his colleagues have speculated: Waller et al., 1998.

131 It wasn’t until about 700 million years ago: Knoll and Carroll, 1999.

131 Soon afterward, animals came on shore: Zimmer, 1998.

131 at least fifty times other lineages of animals followed suit: Poulin, 1998.

133 Attacking people is not how the candiru makes a living: Kelley and Atz, 1964.

133 There you find nests of the ant Tetramorium: Holldobler and Wilson, 1990.

134 Some butterflies, for example, can trick ants: Akino et al., 1999.

135 A single cuckoo starts life much bigger than a warbler: Kilner et al., 1999.

136 The fetus faces the same troubles: Villereal, 1997.

136 This conflict plays out: Pennisi, 1998.

141 Parasites, in other words, have evolutionary stories: Brooks explains how to use this method in Brooks and McLennan, 1993.

142 Tapeworms probably first evolved: Hoberg et al., 1999a.

144 The thorn forests of Bolivia are home to marsupials: For their link to Australian mammals and parasites, see Gardner and Campbell, 1992.

145 Pterosaurs began sharing the sky with birds: Hoberg et al., 1999b.

146 The scenario that reconciles these facts best: Brooks, 1992.

147 The closest relatives to human tapeworms: Hoberg et al., 2000.

148 Suzanne Sukhdeo has sorted through the close relatives: Sukhdeo et al., 1997.

148 Parasitologists have compared species of nematodes: Read and Skorping, 1995.

149 “boring by-product.”: Dawkins, 1990.

149 These are galls: For an overview of galls, see Shorthouse and Roh-fritsch, 1992.

149 Warren Abrahamson of Bucknell University: Abrahamson, 1997.

151 A German evolutionary biologist named Dieter Ebert: Ebert, 1994.

152 And quite often, that optimal virulence: Ebert and Herre, 1996.

154 The biologist Edward Herre studied fig wasps: Herre, 1993.

155 The laws of virulence are also built: Ewald, 1995.

6. Evolution from Within

157 “We behold the face of nature …”: Quoted from Darwin, 1857, p. 116.

158 “Good, when young, bad for the past 33 years.”: Quoted in Adler, 1997.

158 he had Chagas disease: Adler, 1989.

158 Chagas disease is caused by Trypanosoma cruzi: Bastien, 1998.

158 Ticks and lice may only live on their host’s skin: Mooring and Hart, 1992.

159 This sort of monitoring still goes on today: Bingham, 1997.

160 A. R. Kraaijeveld of the Imperial College in England: Kraaijeveld et al., 1998.

163 In only fifty generations: Lively, 1996.

167 It didn’t take Lively long to see a clear pattern: Lively, 1987.

167 In a single lake, they could see parasites: Fox et al., 1996.

168 In Nigeria there lives another snail: Schrag et al., 1994a, 1994b.

168 The most unexpected support for the Red Queen’s effect: Gemmill et al., 1997.

169 It gets into the skin of the rat: Koga et al., 1999.

169 In other words, Strongyloides can complete its life cycle: Viney, 1999.

170 For five years he and another of his postdoctoral students: Dybdahl and Lively, 1998.

171 “I should advise you to walk the other way.”: This parallel between science and literature was nicely observed in Lythgoe and Read, 1998.

172 Hamilton and Zuk gathered together reports: Hamilton and Zuk, 1982.

173 In many of the tests—especially the lab experiments: Clayton, 1991.

173 Zuk studied red jungle fowl from Southeast Asia: Zuk et al., 1995.

173 In a more elaborate study, Swedish scientists: Schantz et al., 1996.

173 That certainly seems to be what’s going on with the fish: Taylor et al., 1998.

174 Immune studies give the Hamilton-Zuk hypothesis: See Møller, 1999.

175 Mice, for example, can smell the urine: Kavaliers and Colwell, 1995a, 1995b.

175 “The scent of a male mouse …”: Penn and Potts, 1998.

175 Bees may be having so much sex: Baer and Schmid-Hempel, 1999.

176 Many insects are shaped expressly to fend off parasites: Gross, 1993.

176 Thousands of species of ants: Feener and Brown, 1997.

178 Mammals are continually assaulted by parasites: The effects of parasites on mammal herds can be found in Hart, 1994, 1997; Hart and Hart, 1994; Hart et al., 1992; Mooring and Hart, 1992.

179 the howler monkeys of Central America: Personal communication, Dr. Katherine Milton.

180 Consider leaf-rolling caterpillars: Caveney et al., 1998.

180 They keep their distance because the manure: Hart, 1997.

181 The odor is like perfume: DeMoraes et al., 1998.

182 Some will just stop eating: Kyriazakis et al., 1998.

182 The woolly bears, in other words: Karban and English-Loeb, 1997.

182 That still gives the snails a month: Minchella, 1985.

183 If a fluke gets into a snail that’s still sexually immature: Lafferty, 1993b.

183 When the fruit flies of the Sonoran desert are attacked by parasites: Polak and Starmer, 1998.

183 Lizards are also tormented by mites of their own: Sorci and Clobert, 1995.

184 Worker bumblebees spend their days flying: Muller and Schmid-Hempel, 1993.

184 When a lungworm drops to the ground in the manure: Robinson, 1962.

186 A new species is born out of isolation: For an accessible overview of speciation, see Weiner, 1994.

186 A parasite that prefers many different hosts: Kawecki, 1998.

187 Lineages of parasites may be able to resist extinction: Bush and Kennedy, 1994.

187 This local struggle: Thompson, 1998.

187 And as these populations of hosts fight off: Thompson, 1994.

188 An interrupted gene may suddenly become able: MacDonald, 1995.

188 The genes that make the receptors: Roth and Craig, 1998.

188 And once a genetic parasite has established itself: DeBerardinis et al., 1998.

189 A bacterium called Wolbachia: See Hurst, 1993; Hurst et al., 1999; Werren, 1998.

7. The Two-Legged Host

192 It’s been worked out best for Trichinella: Bell, 1998.

194 A blood fluke that swam from snails to rats: Despres et al., 1992.

194 The trypanosomes humans had left behind: Stevens and Gibson, 1999.

195 In those early days, parasites did best: Hill et al., 1994.

195 By spreading cats and rats around most of the world: Cox, 1994.

195 Along the Andes, the houses that Incas built: Bastien, 1998.

196 The mosquitoes that carry malaria: Bruce-Chwatt and de Zulueta, 1980.

196 One sort of mutation in the beta chain: Friedman and Trager, 1981.

197 Called ovalocytosis, this disorder: Jarolim et al., 1991; Schofield et al., 1992.

197 One of the few clear signs from antiquity: Senok et al., 1997.

198 And archaeologists in Israel have found bones: Hershokovitz and Edelson, 1991.

199 These mild cases of malaria immunize children: Miller, 1996.

199 In 1990, a biologist named Bobbi Low: Low, 1990.

199 The signs might not be visible either: Penn and Potts, 1998.

200 According to Robin Dunbar: Dunbar, 1996.

201 Sick chimps will sometimes search for strange food: Huffman, 1997.

203 “For the first time it is economically feasible for nations …”: Quoted from Russell, 1955, p. 158.

203 There are more human intestinal worms than humans: These statistics come from Crompton, 1999.

203 Parasites like hookworm and whipworm: Nokes et al., 1992.

204 the disability-adjusted life year: Chan, 1997.

205 Consider the hideous case of guinea worms: Crompton, 1999; Peries and Cairncross, 1997.

205 Seventeen million people carry the parasite: Crompton, 1999.

206 If a person with river blindness takes the drug: Meredith and Dull, 1998.

207 When giant dams are built: Roberts and Janovy, 2000.

207 Chloroquine cures malaria: Ginsburg et al., 1999.

207 Now huge parts of the globe harbor malaria: The spread of resistant malaria is traced in Su et al., 1997.

209 The World Health Organization organized: Wilson and Coulson, 1998.

209 In 1998, human trials began: Shi et al., 1999.

211 These flukes can sense how many: Haseeb et al., 1998.

211 The vaccine could then conceivably cause more harm: Good et al., 1998.

211 Scientists have found that if they give an extra dose: Wynn et al., 1995.

212 If people were vaccinated so that their immune system: Haseeb et al., 1998.

212 One of the architects of the theory of virulence: Ewald, 1994.

214 In 1997, scientists at the University of Iowa: Newman, 1999.

214 Parasite-free living may also be responsible: Bell, 1996; Lynch et al., 1998.

8. How to Live in a Parasitic World

216 “Whenever the earth changed its form …”: Quoted from Farley, 1977, p. 38.

218 Scientists first conceived of using parasites: Two reviews of biological control—both critical—are Howarth, 1991; and Simberloff and Stiling, 1996.

220 It may, for example, have saved much of Africa: The success of the cassava mealybug control program is reviewed in Herren and Neuenschwander, 1991.

231 The forests of Hawaii represent one: Howarth, 1991.

232 In the United States, for example: Boettner, 2000.

233 But if you’re trying to use parasites in the ocean: Lafferty discusses the threat and promise of marine biological control in Lafferty and Kuris, 1996.

238 Ticks can also tamper with our blood: Durden and Keirans, 1996.

239 Only in 1999 did a biologist isolate: Morell, 1999.

240 An ecosystem is a bit like a person: For an introduction to ecosystem health, see Costanza et al., 1992.

241 Parasites are actually a sign: For an overview of parasites and ecological health, see Lafferty, 1997b.

241 Canadian ecologists added lime: Marcogliese and Cone, 1997.

242 Tapeworms may carry hundreds of times: Sures et al., 1999.

243 When ranchers overgraze their cattle and sheep: Grenfell, 1992.

244 a concept, called Gaia, which some scientists embrace: Volk, 1998.