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Comparative Biology of Uncinaria Spp. in the California Sea Lion (Zalophus californianus) and the Northern Fur Seal (Callorhinus ursinus) in California
Abstract
Studies on several aspects of the life cycle of hookworms (Uncinaria spp.) in the California sea lion (Zalophus californianus) and northern fur seal (Callorhinus ursinus) were conducted on material collected on San Miguel Island (SMI), California and at The Marine Mammal Center, Sausalito, California in 1997, 1998, and 1999. Examination of Z. californianus intestines for adult hookworms and feces for eggs revealed that longevity of these parasites in pups is about 6-8 mo, and infections are probably not present in older sea lions. Parasitic third-stage larvae (L3) were recovered from the ventral abdominal tissue of Z. californianus, suggesting transmammary transmission. Callorhinus ursinus pups had no hookworm eggs in their feces or adult worms (except for 1 probable contaminant) in their intestines in the fall and early winter, revealing that adult Uncinaria spp. are spontaneously lost at <3 mo of age of the pups. Sand samples from rookeries, used by both Z. californianus and C. ursinus, on SMI were negative for free-living, L3 in summer months but positive in fall and winter months, indicating seasonality occurred.
... Later, the data were repeated in several checklists and review reports on parasites of marine mammals (Dailey and Brownell, 1972;Margolis and Dailey, 1972;Dailey, 1975;Felix, 2013). Recently, a hookworm recorded from CSLs was extensively studied (Lyons et al., 1997(Lyons et al., , 2000(Lyons et al., , 2011(Lyons et al., , 2016Spraker et al., 2004) and considered as a new species Uncinaria lyonsi (Kuzmina and Kuzmin, 2015). Moreover, CSLs were recently reported to be a new host for Otostrongylus circumlitus (Railliet, 1899) (Kelly et al., 2005). ...
... Hydrurga leptonyx/S Fagerholm and Gibson, 1987;Dailey, 1978;D'Amelio et al., 1994;Zhu et Dougherty and Herman, 1947;Johnson and Ridgway, 1969;Fleischman and Squires, 1970;Dailey, 1970;Dailey and Hill, 1970;Sweeney and Gilmartin, 1974;Schroeder et al., 1973;Ashizawa et al., 1978;Geraci, 1978;Dailey, 1978;Stroud and Dailey, 1978 SP Pseudoterranova decipiens s. l. Pagophilus groenlandicus/ S Herman, 1942, d ;Stroud and Dailey, 1978;Paggi et al., 1991 NS Pseudoterranova azarazi Phoca fasciata/S new host record NS Uncinaria lyonsi (as Uncinaria sp.) CSL/I Dailey and Hill, 1970;Dailey, 1978;Lyons et al., 1997Lyons et al., , 2000Lyons et al., , 2003Lyons et al., , 2016 Ferris, 1916Ferris, , 1934Ferris, , 1951Jellison, 1952;Dailey and Hill 1970;Dailey, 1978 Doetschman, 1944;Newell, 1947;Margolis, 1956;Dahme and Popp, 1963;Dailey and Hill, 1970;Furman, 1977 SP Orthohalarchne attenuata (syn. O. zalophi) ...
... At the same time, pups get infected with nasal mites through direct contact with their mothers and other CSLs (Lyons, personal communication). Hookworms parasitize the pups' intestines up to 7-8 months of age, when the pups start independently feeding on fishes and other preys (Lyons et al., 2000(Lyons et al., , 2016. We did not find U. lyonsi in animals at TMMC, because all of these CSLs we studied were older than 8 months. ...
The population of California sea lion Zalophus californianus (CSL) has steadily increased during the last several decades. Despite extensive research addressing CSL biology and ecology performed during the last decades, there has been a minimal number of published papers documenting their parasite fauna. Our objective was to analyze the actual list of the metazoan parasites reported from CSLs and add new data on the age-related differences in the prevalence and biodiversity of the parasite community. There have been 33 species recorded but this study considers only 24 of them valid. Among them, 11 species are specific parasites of CSLs and 13 species are not specific. Additional species represent accidental infections or misidentifications. In total, 6653 helminths and 847 mites were collected and identified from 34 CSLs for this study. Six species of nematodes, Anisakis simplex sensu lato s. l. (prevalence 41%; intensity 7.6), Contracaecum ogmorhini s. l. (38%; 269.6), Pseudoterranova decipiens s. l. (29%; 33), P. azarazi (9%; 2.7), Acanthocheilonema odendhali (15%; 3.5) and Parafilaroides decorus were found. Two species of cestodes, Diphyllobothrium sp. (38%; 8.5) and Anophryocephalus sp. (15%; 14.6) represent novel undescribed species. Two species of trematodes, Apophallus zalophi (18%; 19.7) and Zalophotrema hepaticum (12%; 39.2), and five species of acanthocephalans, Corynosoma obtuscens (68%; 100.8), C. strumosum (53%; 4.6), Andracantha phalacrocoracis (3%; 1), Andracantha sp. (9%; 4.3) and Profilicollis altmani (6%; 8.5) were found. Mites Orthohalarchne attenuata (prevalence 85%) were found in the nasal cavity, while O. diminuata (21%) parasitized in the trachea and bronchi. The highest levels of infection with nematodes and trematodes were found in adult CSLs (3–16 years old), whereas the highest level of infection with acanthocephalans was found in young CSLs (pups and yearlings).
... In the 2001–2002 and 2002– 2003 seasons, two further epidemics occurred that resulted in the deaths of 32% and 21% of each season's pup production , respectively (Wilkinson et al. 2006); in these instances, the pathogen was the bacterium Klebsiella pneumoniae (Castinel et al. 2007b). Uncinaria sp. have been reported in most otariid species (George-Nascimento et al. 1992; Lyons et al. 2000 Lyons et al. , 2001 Lyons et al. , 2002 Sepulveda 1998), including NZ sea lions (Castinel et al. 2006Castinel et al. , 2007a). Adult hookworms live in the lumen of the intestine of animals where they feed on the mucus, blood and tissue and by doing so, they disrupt the integrity of the sub-mucosal blood vessels. ...
... Depending on the species, the larvae may infect a new host by ingestion, penetration through the skin or via milk. In northern fur seals (Callorhinus ursinus) and Californian sea lions (Zalophus californianus ), hookworm infections have been associated with morbidity and mortality in pups, and are thought to be an inXuencing factor on pup survival, thus acting as a population regulator at some locations where population densities are high (Lyons et al. 2000Lyons et al. , 2001). However, in other otariid species where hookworms are present, hookworms do not occur at the same prevalence and are not considered an important factor for pup mortality and thus population regulation (Sepulveda 1998; Lyons et al. 2002). ...
... This study investigated the eVects of hookworms on early pup growth and mortality in a wild otariid population. In other otariid populations, hookworms have been shown to aVect oVspring mortality and, in some cases, to have density-dependent impacts on breeding populations (Lyons et al. 2000Lyons et al. , 2001 ). However, this is the Wrst study to document the short-term impacts of hookworm infections on growth rates of oVspring. ...
Parasites can have both direct and indirect impacts on organisms through changes in health, growth, reproductive success,
behaviour and survival. This research investigates the effects of hookworms (Uncinaria sp.) on the growth and mortality of New Zealand sea lion (NZ sea lion, Phocarctos hookeri) pups between birth and 3months of age. NZ sea lion pups that received ivermectin treatment to reduce their hookworm burden
had higher growth rates. Hookworm infection had no significant effect on mortality rate except when overall mortality was
high during epidemics caused by other pathogens. Understanding the impacts of parasites on wild populations of pinnipeds is
important for the management of the species, particularly when the species is threatened, as is the case for the NZ sea lion.
There are at least two reasons for this: first, to quantify the impact of the parasite on parameters of population dynamics
such as offspring survival and, as a consequence, female reproductive output; and second, to gain sufficient knowledge of
the host/parasite dynamics to allow the balance to be manipulated in favour of the host should this be required for conservation
management.
... Hookworm-related mortality -uncinariasis: blood loss and enteritis -in pups has been reported in many otariid species including: the California sea lion, Zalophus californianus and Northern fur seal, C. ursinus (Lyons et al. 2000a;, Steller sea lion, ...
... jubatus (Lyons 2005), while much of the reported data come from C. ursinus populations Lyons et al. 2000a;Lyons et al. 2001;. Most recently, the prevalence of hookworm in C. ursinus and Z. ...
... was focused on its life cycle in C. ursinus , which showed that adult worms were shed from pups by the age of 3 months. Further work comparing the biology of hookworms in Z. californianus and C. ursinus showed that the longevity of the parasite in the sea lion pups was 6-8 months (Lyons et al. 2000a). ...
Colony dynamics, maternal investment, and indicators of health were investigated for the New Zealand fur seal (Arctocephalus forsteri) over four austral summers, 2001- 2005. Effort was focused at the Ohau Point seal colony, north of Kaikoura. Two colonies at Banks Peninsula were included for comparisons of colony growth and pup condition. A range of other colonies were also included for making comparisons about colony dynamics and health indices. Colony dynamics were investigated through mark-recapture estimates of pup production and daily census of all individuals at the Ohau Point colony. Maternal attendance patterns were observed through behavioural observations of known females (n = 120), the use of VHF radio transmitters (n = 33), and female mass and body condition estimates (n = 51). Maternal investment was also investigated through longitudinal sampling of pup mass and growth rates. Parameters used to indicate colony health were: body condition, growth, presence of parasites, and the levels and common causes of mortality. The influence of parasites on pup growth was tested using treatment of selected pups with Ivermectin anti-helmentic medication, and mortality in the region was investigated through reports of dead individuals, and post mortems of those found fresh. The Ohau Point colony is in an exponential state of growth, and pup mass and condition was higher and responded to changes in environmental variables differently than at the Banks Peninsula colonies. Lactation lengths were consistently longer at Ohau Point than is typically reported for the species (323-355 days vs. 285 days). Maternal investment strategies were indicative of a close, reliable food source, and showed flexibility between years through extension of foraging trip durations and the increased use of overnight foraging trips. Individual strategies did not significantly influence pup growth. However, increased maternal condition and the ability to respond to inter-annual changes in resource availability resulted in accelerated pup growth even during an El Niño event. The incidence of pups with intestinal parasites was low at Ohau Point, and the average mass of treated and non-treated pups did not differ. Pup mortality in the region was low (3% to 50 days old), however, mortality of older pups was greatly influenced by the proximity of humans, with 2/3 of pup mortality observed between the age of 50 days and weaning being caused by car collisions. The results suggest that population dynamics and maternal investment in the region are greatly influenced by local variables, notably the presence of an accessible food source within close proximity to the colony. Various indicators of health reflect a growing colony in good condition, and the presence of a reliable food source may influence the maximum density and carrying capacity the colony is able to sustain. However, some concerns are raised about the influence of human interactions in the region, and how this may affect mortality and colony dynamics in the future. Extra fencing along the Ohau Point colony is recommended to provide added protection from the road. Continued monitoring of mortality and health indices in the region is also recommended for comparison with other colonies as Ohau Point reaches carrying capacity and density-dependent pressures increase.
... There is currently no evidence that density-dependent factors are operating at the Sandy Bay breeding beach. For example: (1) there is high availability of space for breeding females and pups; and (2) pup mortality is low (averaging 9.7% in the first month of life in the last 11 years excluding episodic mortality events: Wilkinson et al. 2006;Chilvers et al. 2006a) relative to other sea lion species that are showing the effects of known density-dependent factors such as parasite load and hookworm on pup survival (Lyons et al. 2000(Lyons et al. , 2001. Therefore, management of the northern Auckland Island population of NZ sea lions needs to result in an increase in population to a point where the pressures of density dependence at the breeding sites facilitate the dispersal of females to form new colonies, as has been described for other pinniped species (Roux 1987;Gentry 1998;Bradshaw et al. 2000;Gaggiotti et al. 2002;McConkey et al. 2002a). ...
The New Zealand sea lion (NZ sea lion), Phocarctos hookeri, is New Zealand G ÇÖs only endemic pinniped, and one of the worlds rarest otariids. It is classified as G ÇÿThreatened G ÇÖ based primarily on the low number of breeding sites and restricted distribution. In New Zealand, a species listed as G Çÿthreatened G ÇÖ is required to be managed to allow its recovery and removal from the list within 20 years. For NZ sea lions this is dependant on the establishment of new breeding areas. However, understanding the recolonisation processes for pinnipeds is still in its infancy with factors such as philopatry needing more research to understand individual dispersal and the recolonisation process. This paper presents the first quantitative investigation into the level of site fidelity and philopatry to breeding beaches in NZ sea lions. Data from resights of NZ sea lions marked as pups from the northern Auckland Island breeding area suggest that both site fidelity and philopatry are important characteristics of this species. Our results show that overall: (1) females have a higher resighting rate than males, particularly at natal sites; (2) female non-natal resightings are predominantly restricted to locations within the northern Auckland Island breeding area (an area of ~10 km2), whereas male resightings are more widely dispersed (up to 700 km to NZ mainland); and (3) philopatry occurs for both sexes, but is more predominant in females than males, with males displaying delay related to sexual and social maturity. The colonisation of new breeding habitats rarely occurs when philopatry is strong and population density is low, stable or declining such as seen for NZ sea lions. Therefore, this research indicates that management of NZ sea lions needs to minimise anthropogenic mortality and encourage population growth to maximise density at breeding sites and encourage females to disperse to establish new breeding areas.
... The nematodes examined differed morphologically from all nominal species of Uncinaria described from pinniped hosts and appeared to correspond to the form suggested as a separate species in previous studies. Therefore, we present a formal description of the new species of the genus Uncinaria based on morphological investigation of the available material and previously published evidence (Nadler et al., 2000;Lyons et al., 2000;Nadler et al., 2013). ...
A new species of hookworm, Uncinaria lyonsi n. sp., is described based on morphological studies of the nematodes collected by Dr. E. T. Lyons from the California sea lion Zalophus californianus (Lesson) on San Miguel Island, California, USA. The new species is morphologically similar to three other species of the genus Uncinaria Frölich, 1789 parasitising pinnipeds, U. lucasi Stiles, 1901, U. hamiltoni Baylis, 1933 and U. sanguinis Marcus, Higgins, Šlapeta & Gray, 2014, in the body dimensions, the structure of the buccal capsule, the shape and structure of the male caudal bursa and female genital system. Uncinaria lyonsi n. sp. is differentiated from U. lucasi by having longer spicules and gubernaculum, larger buccal capsule and more slender oesophagus. The new species differs from U. hamiltoni and U. sanguinis in having shorter spicules and narrower buccal capsule. The latter two species also occur in the Southern Hemisphere and are geographically separated from U. lyonsi n. sp. The present study confirms the existence of a host-specific species of Uncinaria in the California sea lion, previously revealed by molecular and biological investigations.
... Historically, two species of hookworms of pinnipeds have been described, namely Uncinaria lucasi Stiles, 1901 from the Northern fur seal Callorhinus ursinus (Linnaeus) in Alaska (Olsen & Lyons, 1965) and Uncinaria hamiltoni Baylis, 1933 from the South American sea lion Otaria byronia (Shaw) on the Falkland Islands (Baylis, 1933). Variations in parasite morphology, pathogenicity and life history (Baylis, 1947;Dailey & Hill, 1970;Sepulveda & Alcaino, 1993;Lyons et al., 2000;Beron-Vera et al., 2004;Spraker et al., 2007) have however led to speculation that there may be more than two species. An alternative view is that such variation arises through disparities in environmental influences and that all pinniped hookworms belong to a single species, U. lucasi (see George-Nascimento et al., 1992). ...
This study presents morphological and molecular data on hookworms from the Australian fur seal Arctocephalus pusillus doriferus (Schreber) currently identified in Australian waters as Uncinaria hamiltoni Baylis, 1933. Additional specimens from the Australian sea lion Neophoca cinerea (Péron) and the New Zealand fur seal Arctocephalus forsteri (Lesson) from Australia, and the Southern elephant seal Mirounga leonina (Linnaeus) from Antarctica, were included. Using the internal transcribed spacer (ITS), hookworms from A. p. doriferus, N. cinerea and A. forsteri were found to be genetically similar but distinct from Uncinaria spp. found in M. leonina from Antarctica, as well as from Zalophus californianus (Lesson) and Callorhinus ursinus (Linnaeus) from California. Few morphological differences were detected between these taxa.
... There is currently no evidence that density-dependent factors are operating at the Sandy Bay breeding beach. For example: (1) there is high availability of space for breeding females and pups; and (2) pup mortality is low (averaging 9.7% in the first month of life in the last 11 years excluding episodic mortality events: Wilkinson et al. 2006;Chilvers et al. 2006a) relative to other sea lion species that are showing the effects of known density-dependent factors such as parasite load and hookworm on pup survival (Lyons et al. 2000(Lyons et al. , 2001). Therefore, management of the northern Auckland Island population of NZ sea lions needs to result in an increase in population to a point where the pressures of density dependence at the breeding sites facilitate the dispersal of females to form new colonies, as has been described for other pinniped species (Roux 1987;Gentry 1998;Bradshaw et al. 2000;Gaggiotti et al. 2002;McConkey et al. 2002a). ...
The New Zealand sea lion (NZ sea lion), Phocarctos hookeri, is New Zealand's only endemic pinniped, and one of the worlds rarest otariids. It is classified as 'Threatened' based primarily on the low number of breeding sites and restricted distribution. In New Zealand, a species listed as 'threatened' is required to be managed to allow its recovery and removal from the list within 20 years. For NZ sea lions this is dependant on the establishment of new breeding areas. However, understanding the recolonisation processes for pinnipeds is still in its infancy with factors such as philopatry needing more research to understand individual dispersal and the recolonisation process. This paper presents the first quantitative investigation into the level of site fidelity and philopatry to breeding beaches in NZ sea lions. Data from resights of NZ sea lions marked as pups from the northern Auckland Island breeding area suggest that both site fidelity and philo-patry are important characteristics of this species. Our results show that overall: (1) females have a higher resighting rate than males, particularly at natal sites; (2) female non-natal resightings are predominantly restricted to locations within the northern Auckland Island breeding area (an area of ~10 km 2), whereas male resightings are more widely dispersed (up to 700 km to NZ mainland); and (3) philopatry occurs for both sexes, but is more predominant in females than males, with males displaying delay related to sexual and social maturity. The colonisation of new breeding habitats rarely occurs when philopatry is strong and population density is low, stable or declining such as seen for NZ sea lions. Therefore, this research indicates that management of NZ sea lions needs to minimise anthropogenic mortality and encourage population growth to maximise density at breeding sites and encourage females to disperse to establish new breeding areas.
... This means that pups were not infected from their mothers' milk or by some other route, and therefore, these parasites are not the source of any health issues. As there is no evidence on strict specificity of Uncinaria to pinniped hosts (Lyons et al. 2000; Nadler et al. 2009), it would be of particular interest to examine elephant seal pups in geographical areas where known hookworms exist in other pinnipeds such as California sea lions in Año Nuevo Island or California sea lions and northern fur seals (Lyons et al. 2001) in San Miguel Island, California. This would allow us to study the presence/absence of host specificity of Uncinaria to definite species of pinniped hosts. ...
Northern elephant seals (Mirounga angustirostris Gill, 1866), inhabiting rookeries on the mainland of Año Nuevo State Reserve in central California, were investigated in 2012 for presence of hookworms (Uncinaria spp.). Material collected and examined for hookworms included: blubber (n = 15), stomach and intestines (n = 21) from dead pups; feces from the rectum of weaned pups (n = 23); sand containing apparent feces in areas of weaned pups (n = 28) and sand without apparent feces in areas of weaned pups (n = 54); milk from females (n =23) at 5 days and about 23 to 26 days postpartum; and placenta from one female. Evidence of hookworm presence was not detected in any of the samples examined. Possible reasons why hookworms were not found in northern elephant seals on the mainland of Año Nuevo State Reserve are discussed.
... Data, primarily collected in July and August, on adult hookworms in dead NFS pups on one rookery, or combined with another rookery, revealed prevalences of 79% in , 73% in 1960 , 90% in 1978 , <10% in 1999 , 3% in 2001 , and 6% in 2007 (Lyons et al. 2000a Ionita et al. 2008). The dramatic decline in prevalence and intensity of adult hookworms in pups was reflected in a similar decrease in the number of young males (3 to 4 years old) positive for parasitic L 3 in their blubber. ...
The objective of this article is to review knowledge on the hookworm Uncinaria lucasi Stiles, 1901 in northern fur seals, Callorhinus ursinus Linnaeus, 1758. Emphasis is placed on research on this host-parasite system in the Pribilof Islands, AK, USA where the bulk of the studies has been performed.
Hookworms are blood-feeding nematodes that parasitize the alimentary system of mammals. Despite their high pathogenic potential, little is known about their diversity and impact in wildlife populations. We conducted a systematic review of the literature on hookworm infections of wildlife and analyzed 218 studies qualitative and quantitatively. At least 68 hookworm species have been described in 9 orders, 24 families, and 111 species of wild mammals. Black bears, red foxes, and bobcats harbored the highest diversity of hookworm species and Ancylostoma pluridentatum, A. tubaeforme, Uncinaria stenocephala and Necator americanus were the hookworm species with the highest host diversity index. Hookworm infections cause anemia, retarded growth, tissue damage, inflammation and significant mortality in several wildlife species. Anemia has been documented more commonly in canids, felids and otariids, and retarded growth only in otariids. Population- level mortality has been documented through controlled studies only in canines and eared seals although sporadic mortality has been noticed in felines, bears and elephants. The main driver of hookworm pathogenic effects was the hookworm biomass in a population, measured as prevalence, mean burden and hookworm size (length). Many studies recorded significant differences in prevalence and mean intensity among regions related to contrasts in local humidity, temperature, and host population density. These findings, plus the ability of hookworms to perpetuate in different host species, create a dynamic scenario where changes in climate and the domestic animal-human-wildlife interface will potentially affect the dynamics and consequences of hookworm infections in wildlife.
Necropsy of dead California sea lion (CSL) (Zalophus californianus) pups (n = 20) born in 2014 was done on San Miguel Island, California, in December 2014 and February 2015. The main objective was to obtain data on prevalence/intensity of hookworms (Uncinaria lyonsi) in pups at that time of the year and to compare the results with data from previous studies conducted in December, January, and February. Fourteen dead pups were examined for adult hookworms in December 2014; all pups were infected (prevalence = 100%) with intensity from 6 to 140 (average 58.9 ± 38.9 SD) nematodes per host. Six dead pups were examined in February 2015. Hookworms were present in the intestines of 2 pups (prevalence=33%); two adult female worms were found in each infected pup. From 1 to 23 (average 7.5) parasitic larvae (L3) were found in the blubber of 4 pups. The findings in this study (2014–2015) verify, from earlier observation, that adult U. lyonsi are shed by pups by late February. The prevalence of parasitic L3 in blubber of pups in February has not been previously reported. Sand samples collected in February 2015 from 4 rookery sites were positive for free-living third-stage hookworm larvae, resulting from eggs passed in feces of CSL or northern fur seal pups inhabiting the same rookeries.
Necropsy and extensive parasitological examination of dead northern elephant seal (NES) pups was done on San Miguel Island, California, in February, 2015. The main interest in the current study was to determine if hookworms were present in NESs on San Miguel Island where two hookworm species of the genus Uncinaria are known to be present - Uncinaria lyonsi in California sea lions and Uncinaria lucasi in northern fur seals. Hookworms were not detected in any of the NESs examined: stomachs or intestines of 16 pups, blubber of 13 pups and blubber of one bull. The results obtained in the present study of NESs on San Miguel Island plus similar finding on Ano Nuevo State Reserve and The Marine Mammal Center provide strong indication that NES are not appropriate hosts for Uncinaria spp. Hookworm free-living third stage larvae, developed from eggs of California sea lions and northern fur seals, were recovered from sand. It seems that at this time, further search for hookworms in NESs would be nonproductive.
Context Hookworms (Uncinaria spp.) are a common parasite of neonatal fur seals and sea lions around the world and may contribute to decreased pup growth and survival. Removal of these parasitic burdens by administration of the anthelmintic ivermectin has been trialled in New Zealand (NZ) sea lion (Phocarctos hookeri) pups at Sandy Bay, Enderby Island, with initial benefits in growth and survival reported. Long-term effects, however, are not known. Aims To determine the impact of ivermectin treatment administered in the first month of life, on long-term survival and fecundity in a sample of NZ sea lion pups. Methods For a sample of treated and control pups born between 2002 and 2004, resighting data to 2012 was assessed with the Cox proportional hazards analysis to evaluate survival to maturity and fecundity. Key results Sample size was a limiting factor as juvenile survival was very low, but a trend of improved survival was observed in the ivermectin-treated group. Year of birth was significant due to the effects of a bacterial epizootic in the first year of the trial. Reproductive rate was not significantly different between groups. Conclusions The effect of disease and parasitism on the survival of NZ sea lions is apparent, contributing to early pup mortality, with potentially wider-ranging implications for juvenile survival and beyond. Implications Further research is warranted to investigate anthelmintic treatment of NZ sea lion pups as a safe and effective management tool to improve survival and recruitment in declining populations.
Abstract The hookworms Uncinaria rauschi Olsen, 1968 and Uncinaria yukonensis (Wolfgang, 1956) were formally described from grizzly (Ursus arctos horribilis) and black bears (Ursus americanus) of North America. We analyzed the intestinal tracts of 4 grizzly and 9 black bears from Alberta and British Columbia, Canada, and isolated Uncinaria specimens with anatomical traits never documented previously. We applied morphological and molecular techniques to investigate the taxonomy and phylogeny of these Uncinaria parasites. The morphological analysis supported polymorphism at the vulvar region for females of both U. rauschi and U. yukonensis. The hypothesis of morphological plasticity for U. rauschi and U. yukonensis was confirmed by genetic analysis of the internal transcribed spacers (ITS-1 and ITS-2) of the nuclear ribosomal DNA. Two distinct genotypes were identified, differing at 5 fixed sites for ITS-1 (432 base pairs) and 7 for ITS-2 (274 base pairs). Morphometric data for U. rauschi revealed host-related size differences: adult U. rauschi were significantly larger in black bears than grizzly bears. Interpretation of these results considering the historical biogeography of North American bears suggests a relatively recent host-switching event of U. rauschi from black bears to grizzly bears, which likely occurred after the end of the Wisconsin glaciation. Phylogenetic Maximum Parsimony (MP) and Maximum Likelihood (ML) analyses of the concatenated ITS-1 and ITS-2 datasets strongly supported monophyly of U. rauschi and U. yukonensis, and their close relationship with Uncinaria stenocephala (Railliet, 1884), the latter a parasite primarily of canids and felids. Relationships among species within this group, although resolved by ML, were unsupported by MP and bootstrap resampling. The clade of U. rauschi, U. yukonensis, and U. stenocephala was recovered as sister to the clade represented by Uncinaria spp. from otariid pinnipeds. These results support the absence of strict host-parasite co-phylogeny for Uncinaria spp. and their carnivore hosts. Phylogenetic relationships among Uncinaria spp. provided a framework to develop the hypothesis of similar transmission patterns for the closely related U. rauschi, U. yukonensis, and U. stenocephala.
Secrétariat canadien de consultation scientifique Proceedings Series 2007/005 Série des comptes rendus 2007/005 Proceedings of the workshop on the St. Lawrence Estuary beluga -review of carcass program Compte rendu de l'atelier sur le béluga de l'estuaire du Saint-Laurent – Revue du programme des carcasses November 14 – 17, Route de la Mer / 850, Route de la Mer Mont-Joli (Québec) G5H 3Z4
This paper describes the research activities of the classical Parasitology section of the, over a more than 50 year period. Pioneer research has been conducted on resistance phenomenon against equine small strongyles, sheep stomach worms and equine ascarids. New targets are determining which cyathostomin species are the most resistant to the newest anthelmintic drugs, and what the course of the therapy is. But the paper also describes the wide and important research on endoparasites in otariid pinnipeds conducted by Professor Eugene Lyons and his colleagues in Alaska and California. This paper also presents some of the important publications of the Parasitology section. The Maxwell H. Gluck Center from University of Kentucky, Lexington, has received international recognition for its research dedicated to improving the health and welfare of horses. It is the most important research center on horse problems from all over the world, located in Lexington who's known as "The capital of horses". The Maxwell H. Gluck Equine Research Center is only one of the divisions comprising the Department of Veterinary Science. The others are the Livestock Disease Diagnostic Center and the Equine Parentage Testing and Research Laboratory (Figure 1).
Understanding the fundamental factors influencing the epidemiology of wildlife disease is essential to determining the impact of disease on individual health and population dynamics. The host-pathogen-environment relationship of the endangered Australian sea lion (Neophoca cinerea) and the parasitic hookworm, Uncinaria sanguinis, was investigated in neonatal pups during summer and winter breeding seasons at two biogeographically disparate colonies in South Australia. The endemic occurrence of hookworm infection in Australian sea lion pups at these sites was 100 % and post-parturient transmammary transmission is likely the predominant route of hookworm infection for pups. The prepatent period for U. sanguinis in Australian sea lion pups was determined to be 11-14 days and the duration of infection approximately 2-3 months. The mean hookworm infection intensity in pups found dead was 2138 ± 552 (n = 86), but a significant relationship between infection intensity and faecal egg count was not identified; infection intensity in live pups could not be estimated from faecal samples. Fluctuations in infection intensity corresponded to oscillations in the magnitude of colony pup mortality, that is, higher infection intensity was significantly associated with higher colony pup mortality and reduced pup body condition. The dynamic interaction between colony, season, and host behaviour is hypothesised to modulate hookworm infection intensity in this species. This study provides a new perspective to understanding the dynamics of otariid hookworm infection and provides evidence that U. sanguinis is a significant agent of disease in Australian sea lion pups and could play a role in population regulation in this species.
Infectious disease threatens biodiversity and human health on a global scale, and disease emergence may become more common as humans further encroach on habitats and modify environments. To accurately assess the risk of disease emergence in free-ranging populations of vertebrates, we require an understanding of the dynamics of immunity in the wild. We applied techniques from the emergent discipline of ecological immunology to describe immune activity and dynamics in the endangered Galapagos sea lion Zalophus wollebaeki, which is threatened simultaneously by disease from domestic animals and fluctuations in food supply driven by unpredictable environmental variation. We compared immune activity from shortly after birth until 2 years of age between two Galapagos sea lion colonies: one heavily influenced by humans and the other on an uninhabited island, using a generalized linear model framework. Controlling for development, immune activity was higher in the human-impacted colony, as assessed with both humoural and cellular immune components and cumulative and snapshot measures of immune activity. We discuss the possibility that sea lions in the human-impacted colony are under greater immunostimulatory pressure than those in the comparison colony, which could have implications for individual fitness, colony stability and the risk of disease emergence. The study demonstrates the utility of a generalized and widely applicable approach to quantifying immune activity in wild vertebrates, as it highlights important aspects of the system for targeted analysis and further study. © 2012 The Zoological Society of London.
Practitioners of nematode taxonomy have rarely been explicit about what species represent or how data are being used to delimit species prior to their description. This lack of explicitness reflects the broader species problem common to all biology: there is no universally accepted idea of what species are and, as a consequence, scientists disagree on how to go about finding species in nature. However, like other biologists, nematologists seem to agree that species are real and discrete units in nature, and that they result from descent with modification. This evolutionary perspective provides a conceptual framework for nematologists to view species as independent evolutionary lineages, and provides approaches for their delimitation. Specifically, species may be delimited scientifically by methods that can test the hypothesis of lineage independence. For sequence data, such hypothesis testing should be based on sampling many individual organisms for multiple loci to avoid mistaking tokogeny and gene trees as evidence of species. Evolutionary approaches to analysing data and delimiting species avoid the inherent pitfalls in approaches that use all observed sequence differences to define species through calculation of a genetic distance. To illustrate evolutionary species delimitation, molecular data are used to test the hypothesis that hookworms parasitic in northern fur seals and in California sea lions represent separate species. The advantages and potential caveats of employing nucleotide sequence data for species delimitation are discussed, and the merits of evolutionary approaches are contrasted to inherent problems in similarity-based methods.
We report on the intestinal helminth fauna of 56 South American sea lions, Otaria flavescens, and 5 South American fur seals, Arctocephalus australis, from northern Patagonia, Argentina. A total of 97,325 helminth specimens were collected from sea lions. Gravid individuals were represented by 6 species of parasites: 1 digenean (Ascocotyle (Ascocotyle) patagoniensis), 1 cestode (Diphyllobothrium spp.), 3 nematodes (Uncinaria hamiltoni, Contracaecum ogmorhini s.s., Pseudoterranova cattani) and 1 acanthocephalan (Corynosoma australe). In addition, third-stage larvae of 2 nematodes (Contracaecum sp. and Anisakis sp. type I) and 3 juvenile acanthocephalans (Andracantha sp., Profilicollis chasmagnathi and Corynosoma cetaceum) were also collected. Andracantha sp., C. ogmorhini s.s. and P.
chasmagnathi represent new host records. A total of 1516 helminth specimens were collected from fur seals. Gravid individuals were represented by three species of parasites, namely, Diphyllobothrium spp., C. ogmorhini s.s. and C. australe. In addition, larvae of Contracaecum sp. and P. cattani, juveniles of C. cetaceum and immature cestodes (Tetrabothriidae gen. sp.) were also collected. Corynosoma australe was the most prevalent and abundant parasite in both hosts, accounting for >90% of all specimens. Sea lions and furs seals from northern Patagonia harbour the intestinal helminth communities that could be predicted for otariids, i.e. the combination of species of the genera Corynosoma, Diphyllobothrium, Pseudoterranova, Contracaecum and, in pups, Uncinaria. Additionally, both species of otariid are apparently unsuitable hosts (i.e. non-hosts) for as many as five parasite taxa. The inclusion or exclusion of these species affects estimation of species richness at both component community (11 versus 6 species in sea lions; 7 versus 3 species in fur seals) and infracommunity (mean: 3.1 versus 2.6 in sea lions; 2.2 versus 1.7 species) levels. Information about the reproductive status of helminth species is often lacking in parasitological surveys on otariids and other marine vertebrates, but it is of significance to improve precision in parascript studies or ecological meta-analyses.
The peritoneal cavity (PNC) and intestine of northern fur seal (Callorhinus ursinus) pups and California sea lion (Zalophus californianus) pups that died in late July and early August, 2003, on San Miguel Island, California, were examined for hookworms. Prevalence and morphometric studies were done with the hookworms in addition to molecular characterization. Based on this and previous molecular studies, hookworms from fur seals are designated as Uncinaria lucasi and the species from sea lions as Uncinaria species A. Adult hookworms were found in the PNC of 35 of 57 (61.4%) fur seal pups and of 13 of 104 (12.5%) sea lion pups. The number of hookworms located in the PNC ranged from 1 to 33 (median = 3) for the infected fur seal pups and 1 to 16 (median = 2) for the infected sea lion pups. In addition to the PNC, intestines of 43 fur seal and 32 sea lion pups were examined. All of these pups were positive for adult hookworms. The worms were counted from all but one of the sea lion pups. Numbers of these parasites in the intestine varied from 3 to 2,344 (median = 931) for the fur seal pups and 39 to 2,766 (median = 643) for the sea lion pups. Sea lion pups with peritoneal infections had higher intensity infections in the intestines than did pups without peritoneal infections, lending some support for the hypothesis that peritoneal infections result from high-intensity infections of adult worms. There was no difference in intestinal infection intensities between fur seal pups with and without peritoneal infections. Female adult hookworms in the intestines of both host species were significantly larger than males, and sea lion hookworms were larger than those in fur seals. Worms in the intestine also were larger than worms found in the PNC. Gene sequencing and (RFLP) analysis of (PCR) amplified (ITS) ribosomal DNA were used to diagnose the species of 172 hookworms recovered from the PNC and intestine of 18 C. ursinus and seven Z. californianus hosts. These molecular data revealed that U. lucasi (hookworm of C. ursinus) and Uncinaria species A (of Z. californianus) infrequently mature in the intestine of the opposite host species in California rookeries. However, there is no support from molecular data for the hypothesis that cross-infection with "the wrong" Uncinaria species is a contributing factor in these cases of host peritonitis. The major significance of this research is the unusual finding of adult hookworms in the PNC of so many dead pups. No obvious explanation for this occurrence could be determined. Further research, like in the present study, should help understand and monitor the apparent ever changing role of hookworm disease in the health of northern fur seal and California sea lion pups on SMI.
California sea lions (Zalophus californianus) and northern fur seals (Callorhinus ursinus) are each believed to host distinct hookworm species (Uncinaria spp.). However, a recent morphometric analysis suggested that a single species parasitizes multiple pinniped hosts, and that the observed differences are host-induced. To explore the systematics of these hookworms and test these competing hypotheses, we obtained nucleotide sequences of nuclear ribosomal DNA (D2/D3 28S, D18/D19 28S, and internal transcribed spacer [ITS] regions) from 20 individual hookworms parasitizing California sea lion and northern fur seal pups where their breeding grounds are sympatric. Five individuals from an allopatric population of California sea lions were also sampled for ITS-1 and D18/D19 28S sequences. The 28S D2/D3 sequences showed no diagnostic differences among hookworms sampled from individual sea lions and fur seals, whereas the 28S D18/D19 sequences had one derived (apomorphic) character demarcating hookworms from northern fur seals. ITS sequences were variable for 7 characters, with 4 derived (apomorphic) states in ITS-1 demarcating hookworms from California sea lions. Multivariate analysis of morphometric data also revealed significant differences between nematodes representing these 2 host-associated lineages. These results indicate that these hookworms represent 2 species that are not distributed indiscriminately between these host species, but instead exhibit host fidelity, evolving independently with each respective host species. This evolutionary approach to analyzing sequence data for species delimitation is contrasted with similarity-based methods that have been applied to numerous diagnostic studies of nematode parasites.
A prevalence survey for hookworms (Uncinaria spp.) was done in northern fur seal (Callorhinus ursinus) and California sea lion (Zalophus californianus) pups on San Miguel Island, CA, in 2000. Intestines of dead pups were examined for adult hookworms in July. These parasites were found in 95% of 20 fur seal pups and 100% of 31 sea lion pups. The number of hookworms varied from 4 to 2142 (mean = 760) in fur seal pups and from 20 to 2634 (mean = 612) in sea lion pups. A direct relationship was evident between body condition and number of hookworms in the pups; that is, pups in poor condition had fewer hookworms than those in good condition. There was a decline in the number of hookworms in sea lion pups in 2000 compared to collections in 1996. Eggs of Uncinaria spp. were found in rectal feces (collected in late September and early October) of none of 35 (0%) live fur seal pups and 41 of 48 (85%) live sea lion pups. Packed cell volume values, determined for most of the same live pups, were essentially normal for C. ursinus but were much lower than normal for most Z. californianus. Hookworm larvae were not found in blubber of fur seal and sea lion pups or in rookery sand in July. Rookery sand, positive for live hookworm larvae when put in a refrigerator, was negative at removal 2.5 years later. The average number of eggs in utero of female hookworms was 285 for three specimens from a fur seal pup and 281 from three specimens from a sea lion pup. One hookworm larva was recovered from milk stripped from the teats of a stranded Z. californianus female at The Marine Mammal Center, Sausalito, CA.
Uncinaria spp. were recovered from the milk of California sea lions ( Zalophus californianus) collected from the: (1) teats of a cow just after parturition (one parasitic third-stage larva, L(3)), (2) stomach of her nursing pup (two L(3)), and (3) stomach of a dead pup about 2 days old (one L(3), one headless, probably L(3), and four L(4)) on San Miguel Island, California in May 2001. This, in addition to earlier research, indicates transmammary transmission of hookworms in this host. Uncinaria spp. were found in dead northern fur seals ( Callorhinus ursinus) in the: (1) intestines of 2 of 75 pups (either one or two adult specimens in each infected pup) and (2) ventral abdominal blubber of 3 of 78 subadult males (one to seven L(3) in each infected seal) on St. Paul Island (SPI), Alaska in July and August 2001. These findings verify the low current prevalence of Uncinariaspp. in fur seals on SPI. Rectal fecal samples taken from 50 live Steller sea lion ( Eumetopias jubatus) pups, about 1 month old, on Rogue Reef in Curry County, Oregon in July 2001, were all negative for the eggs of Uncinaria spp. The apparent zero infection rate in these pups is possibly because the rocky terrain of this rookery is not suitable for hookworm transmission.
Neospora caninum is a cyst-forming coccidian that mainly affects bovines, although Neospora infection has also been described in other domestic and wild ruminant species. Serum samples from 78 alpacas (Vicugna pacos) and 73 llamas (Lama glama) at a unique dilution of 1:50 tested by indirect fluorescent antibody test (IFAT) were further analyzed serologically by IFAT and Western blot in both ruminant species to avoid cross-reactions with closely related coccidian parasites and to confirm the existence of N. caninum-specific antibodies. IFAT titers ranging between 1:50 and 1:800 were found. When using Western blot, N. caninum tachyzoite-specific immunodominant antigens with apparent molecular weights of 17-18, 34-35, 37, and 60-62 kDa were also recognized, although some sera with 1:50 IFAT titers proved not to have N. caninum-specific antibodies. As expected, higher IFAT titers were associated with higher anti-N. caninum reactivity in Western blot. This report documents for the first time the presence of N. caninum infection in adult alpacas and llamas from Peru.
Neospora caninum was isolated from the brain of a 6-mo-old aborted bovine fetus from Galicia, Spain. The fetal brain homogenate was inoculated intraperitoneally into cortisonized mice. The peritoneal exudate from the infected mice, along with mouse sarcoma cells (Tg180), was inoculated into a second group of mice, and parasites were harvested from the peritoneal exudate. The parasites were adapted to in vitro growth in Vero monolayers. The tachyzoites from the peritoneal exudate reacted positively with anti-N. caninum antibodies and not with anti-Toxoplasma gondii antibodies on indirect fluorescent antibody test. The tachyzoites were lethal to interferon gamma gene knock out (KO) mice and could be identified immunohistochemically in the tissues. The identity of the parasite was also confirmed by polymerase chain reaction amplification of N. caninum-specific fragments. The sequences of the amplified gene 5 fragments (GenBank AY494944) were found to be identical to that of an Austrian isolate of N. caninum but not to that of NC-1. This is the first isolation of viable N. caninum from Spain.
Thirty-one South American sea lion pups (Otaria flavescens) found dead in Punta León, Argentina, during the summer of 2002, were examined for hookworms (Uncinaria hamiltoni). Parasite parameters were analyzed in 2 locations of the rookery, i.e., a traditional, well-structured breeding area and an expanding area with juveniles and a lax social structure. Prevalence of hookworms was 50% in both localities, and no difference was observed in prevalence between pup sexes (P > 0.05). Hookworms were concentrated in the small intestine. Transmammary transmission is assumed because only adult hookworms were found in the pups. The mean intensity of hookworms per pup was 135; the mean intensity in females (92.78) was significantly different (P < 0.05) from that of males (230.25). No difference (P > 0.05) in intensity was found between the 2 breeding areas, although prevalence was higher in the traditional breeding area than in the other area. Location was the only factor affecting hookworm prevalence (P log-linear model: 0.9552; chi2: 1.5629). No apparent trend between body condition and intensity of hookworms was observed.
Intestines of California sea lion (Zalophus californianus) pups (n= 204), born in 2002 on San Miguel Island, California, were examined for hookworms (Uncinaria spp.) as part of a seasonal mortality study from June through December 2002 and January 2003. The investigation was planned to coincide with most of the previously established hookworm infection period of the pups. Prevalence of hookworms in dead pups was 100% for each month of the study. The geometric mean intensity of infections per month was: 94.03 (n=30) for June, 629.09 (n=50) for July, 319.90 (n=31) for August, 159.90 (n=30) for October, 109.03 (n=30) for November, 37.84 (n=24) for December 2002 and 11.05 (n=9) for January 2003. In addition to the temporal pattern, the infection intensity was higher for pups in good condition and for male pups. An inter-year comparison of hookworm counts from dead pups collected in July of 1996, 2000, and 2002 also demonstrated higher intensity in pups in better condition but sex-differences in intensity were inconsistent across years. The inter-year comparison also demonstrated higher intensities in dead pups collected from portions of the rookery with sandy substrate versus rocky substrate. No annual differences in intensity were found after adjusting for substrate and condition.
Low genetic heterozygosity is associated with loss of fitness in many natural populations. However, it remains unclear whether the mechanism is related to general (i.e. inbreeding) or local effects, in particular from a subset of loci lying close to genes under balancing selection. Here we analyse involving heterozygosity-fitness correlations on neonatal survival of California sea lions and on susceptibility to hookworm (Uncinaria spp.) infection, the single most important cause of pup mortality. We show that regardless of differences in hookworm burden, homozygosity is a key predictor of hookworm-related lesions, with no single locus contributing disproportionately. Conversely, the subsequent occurrence of anaemia due to blood loss in infected pups is overwhelmingly associated with homozygosity at one particular locus, all other loci showing no pattern. Our results suggest contrasting genetic mechanisms underlying two pathologies related to the same pathogen. First, relatively inbred pups are less able to expel hookworms and prevent their attachment to the intestinal mucosa, possibly due to a weakened immune response. In contrast, infected pups that are homozygous for a gene near to microsatellite Hg4.2 are strongly predisposed to anaemia. As yet, this gene is unknown, but could plausibly be involved in the blood-coagulation cascade. Taken together, these results suggest that pathogenic burden alone may not be the main factor regulating pathogen-related mortality in natural populations. Our study could have important implications for the conservation of small, isolated or threatened populations, particularly when they are at a risk of facing pathogenic challenges.
This is the first investigation of the epidemiology of hookworm (Uncinaria spp.) infection in New Zealand sea lions (NZSLs; Phocarctos hookeri) on Enderby Island, Auckland Islands. The examination of faeces for hookworm eggs in various age categories of sea lions revealed that only pups up to at least 3 months of age harboured adult hookworms in their intestines. Gross necropsy of more than 400 pups from 1999/2000 to 2004/2005 showed that the prevalence of hookworm infection varied significantly between years and was higher from mid-January to the end of February when the majority of pups were between 3 and 9 weeks old. The average burden of adult parasites per pup was not influenced by the host's sex and body condition or by year. This study also provided evidence for transmission occurring by the transmammary route in NZSLs.
Hookworms in otariids are considered to meet the conditions and to fulfill the predictions set forth in the theoretical literature to define a likely case of host coexistence mediation by a shared pathogen. The intensity of infections, the prevalence of skin lesions and the morphometry of hookworms Uncinaria spp. were examined in South American sea lions and fur seals sampled along the Chilean and the Uruguayan coasts in spring and summer 1981 to 1991. In sympatric host populations from Uruguay, there were clear differences in intensity of infections, prevalence of skin lesions, and body size of the hookworms from the two host species. Sea lions from Chile, allopatric to fur seal populations, are less intensively infected and hookworms found in these sea lions have the smallest body size reported in otariids, while those from South American fur seals are the largest. Hookworms found in sea lion pups from populations sympatric to fur seals revealed intermediate values in intensity and in body size, and the sea lion pups had the highest prevalence of skin lesions. Other reports of hookworms in otariids show intermediate morphometry, following a general linear trend of differentiation in size. Consequently, they are considered to belong to the same, widely distributed species Uncinaria lucasi Stiles, 1901.
Twelve fur seal pups, which had not nursed their mothers, were used in an infectivity experiment. Pups were exposed to parasitic 3rd-stage larvae of Uncinaria lucasi from belly tissues of fur seal bulls, bachelors, and pregnant cows, to determine maturation capability of the larvae. Hookworms were not recovered from the intestines of 3 pups receiving larvae from belly blubber of bulls, 6 pups receiving larvae from belly blubber of bachelors, and 1 nonexposed pup. Maturation of hookworms did occur in 2 pups exposed to larvae from a mixture of belly blubber, mammary tissue, and milk of pregnant cows. Parasitic 3rd-stage hookworm larvae from belly tissues of pregnant and "non-pregnant" fur seal cows averaged 938.1 and 802.1 micron long, and 34.1 and 31.5 micron wide, respectively; however, larvae from belly tissues of a fur seal bull, bachelors, 2-year-old males, male and female yearlings and pups, and Steller Sea Lion subadults averaged 640.5-732.0 micron long and 20.9-24.9 micron wide.
This chapter discusses the life cycle of Uncinaria lucasi in fur seals, which consists of three basic parts: (1) the free-living phase with eggs and free-living third-stage larvae in the soil, (2) the tissue phase wherein parasitic third-stage larvae occur in all age groups of seals, and (3) the intestinal phase consisting of fourth-stage larvae, adolescent, and adult worms occurring in the intestine of young pups. Infection of all seals with the tissue phase is primarily by the percutaneous route but may occur per os, entry being mainly through the flippers. Infection of young pups with the intestinal phase is through the parasitic third-stage larvae, which are passed postpartum in the milk for only a short time. Almost all young fur seal pups born on the Pribilof Islands become infected with adult hookworms in the ileo-caecal region of the intestine by the time they are two weeks old. This life cycle is unique among those known for the helminthes in that adult worms occur in the intestine of only very young pups, and the infective stage that develops to adulthood is transmitted in the milk during the first few days postpartum only.
Northern fur seal (Callorhinus ursinus) (n = 25) and California sea lion (Zalophus californianus) (n = 53) pups, found dead on rookeries on San Miguel Island (California, USA), were examined for adult Uncinaria spp. Prevalence of these nematodes was 96% in fur seal pups and 100% in sea lion pups. Mean intensity of Uncinaria spp. per infected pup was 643 in fur seals and 1,284 in sea lions. Eggs of Uncinaria spp. from dead sea lion pups underwent embryonation in an incubator; development to the free-living third stage larva occurred within the egg. This study provided some specific information on hookworm infections in northern fur seal and California sea lion pups on San Miguel Island. High prevalence rate of Uncinaria spp. in both species of pinnipeds was documented and much higher numbers (2X) of hookworms were present in sea lion than fur seal pups.