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ABSTRACT
Sixty Juan Fernández fur seal pups (Arctocephalus philippii) found dead on Alejandro Selkirk Island, Chile, during the breeding seasons of 1991 and 1992 were examined for the presence of hookworms (Uncinaria sp.). Hookworms were found in 60% of the pups examined, at a mean intensity of 17 parasites per infected host. Intensity of infection did not differ among years or sexes. There was a significant positive relationship between thickness of subcutaneous fat and number of hookworms.
    The Juan Fernández fur seal (Arctocephalus philippii Peters) is endemic to the Juan Fernández Archipelago, 800 km off the coast of central Chile. Until the last century, Juan Fernández fur seals were very abundant, numbering in the millions (Hubbs and Norris, 1971). As a result of intense hunting during the 1700 and 1800s, however, population numbers were so reduced that in 1880 the species was thought to be extinct. Since its rediscovery in 1965, this population of fur seals has grown from about 200 to more than 4,500 animals (Torres, 1987).
    There are only 2 reports on the helminth fauna of Juan Fernández fur seals (Cattan et al., 1980; Sepúlveda and Alcaíno, 1993). Hookworms (identified as Uncinaria hamiltoni Baylis, 1933) were reported for the first time from pups of this species in 1990 (Sepúlveda and Alcaíno, 1993). In that study, 6 of the 20 pups examined were infected with hookworms (range of 3-63 parasites per pup). George-Nascimento et al. (1992) recently suggested, however, that all hookworms reported in pinnipeds belong to 1 species, Uncinaria lucasi Stiles, 1901. These authors compared several morphometric characters from Uncinaria sp. hookworms from 4 species of otariids (from both the northern and southern hemispheres) and observed a general linear trend of differentiation in size with a wide overlap in body measurements. Because of this uncertainty, hookworms in this paper will be referred to as Uncinaria sp.
    In the present study, information on the prevalence and intensity of hookworm infections in Juan Fernández fur seals found dead at Alejandro Selkirk Island, Chile, was obtained. Data for the intensity of infection with this parasite between years and pups of different sexes and body conditions were compared and examined within the context of information on hookworms in other pinnipeds.
    Field work was conducted at Alejandro Selkirk Island, Juan Fernández Archipelago, Chile (33°45'S, 80°45'W), during the breeding seasons for Juan Fernández fur seals (late Novemberlate January, 1991 and 1992). Necropsies were performed on 60 fur seal pups found dead in the rookery. The sample included 33 females and 27 males weighing a mean of 5.3 +/- 1.8 kg (range, 2-11.4 kg). Pups were between 0 and approximately 45 days of age. The complete gastrointestinal tract (esophagus to rectum) was examined for the presence of parasites. The intestine was opened with scissors, scraped, and washed; the washings were then screened through a 150-µm sieve, and all material remaining in the sieves was examined. All nematodes were collected, counted, preserved in 70% alcohol, and in the laboratory cleared in lactophenol for identification. Animals were assigned to 1 of 3 body condition categories on the basis of thickness of subcutaneous fat (measured on the midline on midsternum). The categoires included slight to no fat (0-0.7 cm), moderate fat (0.8-1.5 cm), and abundant fat (1.6-2.3 cm). Voucher specimens of nematodes have been deposited in the U.S. National Parasite Collection, Beltsville, Maryland (USNPC 87637).
    Kruskal-Wallis tests were used to evaluate differences in intensity of infections between years, sexes, and amount of subcutaneous fat of the pups (SAS Institute Inc., 1988). The terms, prevalence, intensity, and mean intensity follow the definitions given by Bush et al. (1997).
    Cause of death was determined in 44 of the 60 pups examined and included trauma from intraspecific aggression (38%), starvation (28%), and handling (7%). Small intestines of pups were infected only with Uncinaria sp. at a prevalence of 60% (36/60 pups examined, both years combined). No parasite was collected from the esophagus, stomach, or large intestine of pups. Hookworms were not associated with any gross pathology and thus were not implicated as a cause of mortality in any of the pups examined. Mean intensity of hookworms per infected pup was 17 +/- 36 (mean +/- SD; range 1-151), a much lower value when compared with northern fur seal (Callorhinus ursinus Linnaeus) and California sea lion (Zalophus californianus Lesson) pups from California (mean intensities of 643 and 1,284, respectively; Lyons et al., 1997). In Alaska, Olsen (1958) reported a higher prevalence and mean intensity of infection in northern fur seal pups from sandy rookeries compared with nonsandy ones and concluded that this difference was related to a higher survival of eggs and larvae in the sandy soils. Whether the absence of sandy rookeries on Alejandro Selkirk Island could explain the lower number of parasites per infected host found in Juan Fernández fur seals is not known.
    Sex of the animals had no significant effect on the number of parasites present (mean intensities of infection of 13 +/- 19 and 21 +/- 39 for male and female pups, respectively; Kruskal-Wallis test, H = 0.166, df = 1, P = 0.683). Similarly, there was no difference in the intensity of infections between years (mean intensities of infection of 9 +/- 18 and of 27 +/- 41 for 1991 and 1992, respectively; Kruskal-Wallis test, H = 2.103, df = 1, P = 0.147).
    There was a significant positive relationship, however, between the amount of body fat and number of hookworms, i.e., pups with abundant subcutaneous fat possessed the highest numbers of nematodes (Kruskal-Wallis test, H = 18.33, df = 2, P = 0.0001; Table I). Olsen (1958) also reported this phenomenon in northern fur seals and noted that pups "heavily" parasitized by U. lucasi were generally fat and in excellent physical condition. More recently, Lyons et al. (1997) reported a similar trend in pups of California sea lions infected with Uncinaria spp. but failed to find any difference in the number of hookworms in relation to body condition in pups of northern fur seals. The fact that animals in good nutritional condition had higher numbers of Uncinaria sp. could be explained by the life cycle of these parasites. In northern fur seals, the life cycle of U. lucasi has been well documented, and larvae are transmitted to newborn pups through the milk by their mothers, mainly during early lactation (Olsen and Lyons, 1965). In Juan Fernández fur seals, there is also evidence of transmammary passage of hookworm larvae (Sepúlveda and Alcaíno, 1993). In the present study, heavier intensities of hookworms in "fatter" pups could be directly related to a higher consumption of milk at an early age and thus to a higher ingestion of larvae.
    In pups of Juan Fernández fur seal, hookworms were distributed throughout the small intestine, but they were found mainly in the duodenum and jejunum. In many cases, female and male worms were copulating and still attached to the mucosa of the small intestine when collected. The relatively low intensity of infection with Uncinaria sp. and the absence of lesions in the small intestine of these pups are indications that, presently, hookworm infections are probably not an important cause of mortality in this species of pinniped.
    This study was partially funded by grants from The Smith-sonian Institution and The National Geographic Television awarded to John M. Francis. Assistance in the field was provided by Hugo Ochoa-Acuña, John Francis, Hernán Díaz, and by staff from the Corporación Nacional Forestal, Juan Fernández Archipelago, Chile. Donald J. Forrester critically reviewed the manuscript.
ADDED MATERIAL
    María Soledad Sepúlveda, Department of Physiological Sciences, College of Veterinary Medicine, University of Florida, Gainesville, Florida 32611
    TABLE I. Prevalence, range, and mean intensity of hookworm infections (Uncinaria sp.) in pups of Juan Fernández fur seals (Arctocephalus philippii) in relation to amount of subcutaneous fat.

 Amount of           Prevalence %
subcutaneous       (number infected/                 Intensity
     fat           number sampled)        Range    (mean +/- SD)
Abundant             93 (29/31)           1-151      29 +/- 38
Moderate             30 (3/10)            2-83       10 +/- 26
Slight to none       21 (4/19)            6-23        3 +/- 7
Overall              60 (36/60)           1-151      17 +/- 32

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