Biology 625
ANIMAL PARASITOLOGY
Fall semester lecture note outline

Updated: 25 June 2001

1. Considered to be at least 4 unique parasite species specific for each host, suggesting that at least 80% of all species of organisms are parasites (May, 1992, Sci Am 267: 42-48). This is most likely an under representation. Humans are known to be infected by nearly 400 non-arthropod parasitic species; some species host specific only for humans.
2. All parasites are heterotrophs and at least primary consumers; some are much higher on the food pyramid.
3. The plane of host nutrition may affect parasite growth and fecundity. However, these effects depend on the species involved. For instance:
   1. Reduced nutrition reduces fecundity of blood flukes in humans (Anderson and May, 1991, Infectious diseases of humans, Oxford)
   2. Reduced nutrition increases fecundity of intestinal helminths in humans (Anderson and May, 1991, Infectious diseases of humans, Oxford).
4. Parasites may reduce host fitness and reduce fecundity in many instances:
   1. Saumier et al. (1988, Can J Zool 66: 1685-1692) found American kestrels infected with Trichinella pseudospiralis flew less and underwent less preening behaviour than uninfected control birds.
   2. Saumier et al (1986, Can J Zool 64: 2123-2125) found American kestrels infected with T. pseudospiralis produced an average of 0.6 hatchlings compared to 2.1 hatchlings for uninfected controls. Infections did not affect the birds to produce their first 3 eggs but significantly reduced their ability to produce additional eggs
   3. Hudson (1986, J Anim Ecol 55: 85-92) and Hudson et al. (1992, J. Anim Ecol, 61: 477-486) found that grouse treated annually with antihelminthics consistently had statistically higher clutch sizes and surviving offspring than birds with natural burdens.
   4. Grouse in the UK show 4-5 year cyclic population crashes. Grouse on English estates treated with levamisole, an anti-helminthic against Trichostrongylus tenuis, showed a 44% decrease in numbers during crash years compared to birds on untreated estates with a 97% decrease.
   5. Mice infected with Trichinella spiralis reveal decreased dominance status than uninfected mice (Rau, 1983, Parasitology, 86: 319-322).
5. Parasites may alter host behavior
   1. Cockroaches infected with Moniliformis moniliformis move slower, pause for longer periods of time, but actually spend more time moving, than uninfected roaches. Infected arthropods were also more positively phototaxic, and spend more time on horizontal surfaces, than do uninfected controls (Moore, 1983, J Parasitol 69: 1174-1176; 1984, Am Nat 123: 572- 577). This all allows them to be more easily eaten by definitive hosts
   2. The muskrat and surface-feeding duck acanthocephalan, Polymorphus paradoxus, changes the crustacean intermediate host phototaxis from negative to positive (Maynard et al. 1996, J Parasitol. 82: 663-666). Injection of serotonin into uninfected crustacea also results in similar results (Helluy and Holmes, 1990, Can J Zool 68: 1214-1220).
   3. The starling acanthocephalan, Plagiorhynchus cylindraceus, causes the isopod intermediate host to spend more time on light-colored surfaces and in unsheltered areas than uninfected isopods (Moore, 1983, Ecology 64: 1000-1015).
   4. Metacercariae of Brachylecithum mosquensis encyst near supraesophageal ganglia of carpenter ants causing them to seek brightly lit areas and wander aimlessly rather than seek dark areas. This makes infected ants more available to American robins (Carney, 1969, Am Midland Nat 82: 605-611).
   5. Metacercariae of Dicrocoelium dendriticum encyst near subesophageal ganglia of Formica spp. ants causing them to climb to the tops of grasses in the low temperatures of the evening and grasp the plant firmly with mandibles. Ants remain attached until the next morning, when the temperature (Anokhin, 1966, Dokl Akad Nauk SSR 166: 757-759; Hoborst, 1964, Z Parasitenkd 22: 105-106; Spindler et al. 1986, Z Parasitenkd 72: 689-692)
   6. Mice infected with Toxocara canis have increased running activity, presumably resulting in mice becoming more vulnerable to canids (Hay et al. 1985, Ann Trop Med Parasitol 79: 221-222).
6. Numbers of parasites highly variable among individuals within a host population. This is due to multiple factors including:
   1. Individuals have differential exposure to infective stages; accounts for much of the variation.
   2. Individual animal physiology/genetics account for considerable variation.
   3. However, even when genetics and immunology carefully controlled experimentally, still much unexplained variation among individuals.
   4. Host behavior also accounts for variation in numbers of parasites per individual in a population (below). Important to remove, destroy, or avoid parasites.
      1. Swatting flies and other flying insect repelling behavior
      2. Preening to remove mites, lice, and fleas, as well as mutual and self grooming
      3. Avoidance of foods containing parasite eggs or larvae
      4. Habitat and nest avoidance or modification
      5. Perhaps acquisition of insect repellants, i.e. anting, but this is still under investigation
      6. Sexual selection and rejection of parasitized mates.
         1. Assumes individuals carry genes for resistance to parasites.
         2. Assumes animals can identify potential mates that are infected.

Repelling behaviour

1. Includes head shaking, tail swatting, foot stamping, bill snapping, wing flapping.
2. Edman et al. (1974, J Parasitol, 60: 874-883) and Scott and Edman (1991, Parasite-bird interactions, Oxford, 179-204) found that mammal and bird species with higher numbers of anti- mosquito movements per hour had fewer bites. They also found that anti-mosquito movements increased with exposure to mosquitos.
3. It has been assumed, but not completely studied, that birds place exposed portions of body under plumage, including head and legs, during sleeping.

Grooming and preening

1. Birds spend about 10% of their time grooming
2. Brown (1974, Poultry Science, 53: 1717-1719) found that chickens infested with lice preened 5-10x times the rate of uninfested chickens.
3. Clayton and Cotgreave (1994, Animal Behaviour, 47: 195-201) found birds with unwieldy bills spend significantly more time scratching with their feet than sister taxa with shorter bills.
4. Clayton (1991, Parasite-bird interactions, Oxford, 258-289) found that a house sparrow missing part of its upper beak had 10x more lice and mites than other sparrows.
5. Nelson and Murray (1971, Int J Parasitol 1: 21-29) clipped 1 cm from the beak tips of pidgeons and found lice on these birds to increase to uncountable levels within 1-2 mos.
6. Brown (1972, Poultry Science, 51: 162-164) found chickens with clipped beaks grew thousands more lice within 30 days than control birds.
7. Brooke (1985, Auk, 102: 893-895) found that mated pairs of Antarctic eudyptid penguins allopreen (mutually preening) whereas non-mated birds do not allopreen. Allopreening resulted in 2-3x fewer ticks around the head and neck as opposed to unmated birds. Mated and unmated birds spent the same amount of time self-preening.

Heterospecific cleaning

1. Oxpeckers of Africa favor animals with the highest tick densities, and numbers of tick birds per unit area of body correlates to tick density. Animals often behave characteristically to facilitate cleaning (Hart et al. 1990, African J Ecol, 28: 240-249; Mooring and Munday, 1996, African J Ecol, 34: 54-65).
2. Cowbird chicks clean bot fly larvae from host chicks. Two host birds in South America fledge more chicks when a cowbird is present than when the cowbirds are not present. In addition, adults with nests with high bot fly probability made no attempt to drive away cowbird females nor did they expel cowbird eggs (Smith, 1968, Nature, 219: 690-694).
3. Since eastern screech owls use the same nests repeatedly, large numbers of ectoparasites can build up. Adults owls release live blind snakes into the nest that often remain and feed on fly larvae and other arthropods. Nestlings with live-in blind snakes grow faster and have lower mortality than nestlings in the absence of blind snakes (Gehlbach and Baldridge (1987, Oecologia, 71: 560-563).

Birds and nest-borne parasites

1. Nests serve as a dark, warm, and stable with an abundant food supply
2. Good breeding ground for mites, bugs, fleas, ticks, dipteran larvae, and lice
3. Long term and year-to-year occupancy results in heavy parasite burdens
4. Birds face the dilemma
   1. Build new nests each year to help avoid parasite build-up, although must expend extra energy to build the new nests
   2. Re-use nests year-to-year, which results in parasite build-up but reduces amount of energy expended in nest building
5. Some sample solutions
   1. Loye and Carroll (1991, Parasite-bird interactions, Oxford, 222-241) found that cliff swallows use same nests every other year (as opposed to every year) where blood sucking hemipterans were a problem
   2. Christie et al. (1994, Animal Behaviour, 47: 895-898) found that greater tits are able to avoid nests with fleas and select nests without fleas
   3. Duffy (1983, Ecology, 64: 110-119) found that sea birds avoid build-up of tick numbers in nests by nesting early in the year before tick numbers have a chance to build up.
   4. Incorporate insecticidal nesting material, especially in avian species that reuse nests year-to- year.
      1. Sengupta (1981, Emu, 81: 114-115) found sparrows in India incorporated maragosa leaves in their nests, which contain natural insecticides.
      2. Clark and Mason (1985, Oecologia, 67: 169-176) found that preferred plants, such as wild carrot and flea bane, contain substances that retard hatching of louse eggs in starling nests.
      3. Clark and Mason (1985, Oecologia, 67: 169-176) noted that removing fresh plant materials from starling nests resulted in significant increases in nest mites
   5. Duffy (1983, Ecology, 64: 110-119; 1991, Parasite-bird interactions, Oxford, 242-257) found that seabirds nest near guano accumulations, which contain ammonia and inhibit nest dwelling arthropods

Avoidance - of food containing parasites or eggs or habitat with parasites

1. Most examples in the literature have shown that parasites actually have ways to enhance hosts to eat eggs or larval stages. Food avoidance examples rare in the literature.
2. Moore (1983, Ecology 63: 1000-1015) found isopods tended to avoid starling feces containing acanthocephalan eggs.
3. Oyster catchers tend to avoid trematode infected bivalve intermediate hosts in intertidals. Infected molluscs tend to burrow in the sand nearer to the surface than uninfected molluscs (Lim and Green, 1991, Can J Zool 69: 2202-2208).
4. Downes et al. (1986, Can J Zool, 64: 622-629) has shown caribou avoid high densities of mosquitos by moving to higher altitudes during summer grazing.

Sexual selection of uninfected mates

1. 3 models of parasite-mediated sexual selection
   1. Females benefit by mating with low or non-parasitized males. This increases chances of parasite any resistant genes being passed to offspring.
   2. Females that avoid mating with parasitized males decrease chances of directly picking up contagious parasites.
   3. Females gain direct benefit since low or non-parasitized males should provide better mate and nest guarding, as well as better parental care, than parasitized males
2. Many studies have failed to find any correlation between male reproductive success and specific parasitism. However, other studies have found a correlation in some host species with some parasites.
   1. Peirce (1989, Disease and threatened birds, ICBP Tech Publ 10: 69-76) found avian malaria in grouse lowered lek attendance when compared to uninfected birds.
   2. Johnson and Boyce (1991, Parasite-bird interactions, Oxford, 377-388) found male sage grouse with fewer ectoparasites mated more frequently than heavily infected males.
   3. Zuk et al. (1990, Am Zoologist 30: 235-244) found red jungle fowl experimentally infected with intestinal nematodes had smaller combs and mated less frequently than uninfected control birds.
   4. Clayton (1990, Am Zoologist 30: 251-260) found male rock doves infested by chewing lice displayed poorly and were discriminated against by females.
   5. Moller (1990, Evolution, 44: 771-784; 1991, Parasite-bird interactions, Oxford, 328-343) noted unmated male barn swallows were more heavily infected with mites and lice than mated males and that resistance to mites was heritable. Parents with longer tails produced offspring that had significantly fewer mites even when offspring reared by foster parents.
   6. Hillgarth (1990, Am Zoologist, 30: 227-233) found male pheasants with heavy coccidial loads had less colorful wattles and mated less frequently than lightly infected males. However, offspring of heavily infected pheasants had more robust offspring.

NOTE: Portions of the above were adapted from Clayton, D. H., and J. Moore (eds.). 1997. Host-Parasite Evolution: General Principles and Avian Models. Oxford University Press. 450 pp. If you have an interest in ecology of parasitism, this book contains a large amount of information.