Mating of Ancylostoma caninum in Relation to Blood Loss in the Host

Abstract

By oral inoculation of juvenile or adult worms, unisexual or bisexual Ancylostoma caninum infections were established in 39 young dogs. Less than 100 adult females caused rapid blood loss and anemia in two dogs at the time when the worms began laying infertile eggs. Equally heavy all-male or balanced male-female infections did not cause detectable anemia. A higher percentage of males remained in recipient dogs when transferred with (62%), than without (49%), females, but females became established equally well with or without males (average 55%). The average rate of laceration (per 100 worms) was greatest in all-female (147) and unbalanced infections (97 and 134), least in all-male infections (21), and relatively low but highly variable in balanced infections (57, range 3 to 122). Laceration rate was not related to overall population density, but when worms were very unequally distributed as they often were in all-female infections, or bunched as they were when males congregated around receptive females, the focal laceration rates were high. Blood in the worm's intestine was evident more frequently in females than in males, being seen in 53, 64, and 80% of females in balanced, unisexual, and unbalanced infections, respectively. The corresponding rates for males were 26, 9, and 37%. More than half of the worms of both sexes were unattached to the intestinal mucosa when observed 15 to 30 min after death of the host through Nembutal injection into the heart. The observations suggest that the female of A. caninum normally mates at intervals of 3 weeks or less, that mating behavior is attendant with laceration of the intestinal mucosa, especially when the sexes are highly unbalanced, and that mating may rank high among those activities of the hookworm which cause blood loss and anemia in the host. It is generally accepted that hookworms cause anemia and that the anemia results directly from blood losses caused by the worms. In the freshly opened intestine of infected dogs, blood is often seen oozing from the lacerated mucosa and filling the intestine of the hookworms. Estimates have been made of the amounts of blood passing daily through the intestine of hookworms (Wells, 1931) and the daily losses of blood into or from the intestine of the host (Roche, 1957a, b; Foy et al., 1958; Clark et al., 1961). The rate of blood loss and the consequent anemia are, in general, proportional with the number of worms present in the intestine. In extreme cases this relationship is clear and indisputable. In some instances, however, the Received for publication 6 December 1963. * Supported by Grant AI-04919 from the National Institutes of Health, U. S. Public Health Service. t Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kawara-machi, Kamikyo-ku, Kyoto, Japan. relationship between worm burden and blood loss or anemia is not evident, and the lack of such a relationship cannot always be explained on the basis of duration of infection or nutriional status of the host (Foy and Kondi, 1960, 1961). The present study was undertaken to examine the possible role of sex and mating behavior of Ancylostoma caninum in the causation of blood loss in the dog. MATERIALS AND METHODS Thirty-nine mongrel dogs 3 months to approximately 6 months of age were caged separately, given a ration of commercial canned dog food, treated for helminths until stools were negative (by zinc sulfate flotation) for a period of at least 15 days, and given infections with adult or adolescent worms of predetermined number and sex. Adult worms carefully removed from freshly killed, naturally infected dogs, or adolescent worms 7 to 11 days of age, similarly taken from experimentally infected dogs, were examined individually under suitable magnification to determine the sex. Counted numbers of the worms were then transferred to 1-ml gelatin capsules and placed over the glottis of a recipient dog. Usually the capsules were