The diversity and impact of hookworm infections in wildlife

Abstract

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.

The contrasting hidden consequences of parasitism: Effects of a hematophagous nematode (Uncinaria sp.) in the development of a marine mammal swimming behavior

“…Additionally, a higher proportion of hookworm‐infected pups engaged in swimming compared to noninfected pups. These observations are the opposite of our predicted impact of hookworms in the development of swimming skills given the known effects of hookworms on body mass and hemoglobin levels (Seguel & Gottdenker, ). An alternative explanation for these results can be given by a potential compensatory mechanism deployed by fur seal pups with hookworm infection.…”

“…However, detecting these dynamics in natural systems is challenging because the impact of parasites on host populations is sometimes subtle and difficult to document (Pedersen & Fenton, ). These subtle or “hidden effects” of parasitism are hard to measure because they are associated with changes in behavior and physiological variables which may be affected by factors other than parasitism (e.g., diet, maternal care, genetics) (Carlsson et al, ; Higgins & Gass, ; Seguel & Gottdenker, ). Additionally, the changes in an animal physiology and health status due to parasitism are related not only to the parasite but also to the host response to the infection (Ezenwa et al, ; Fox, ; Seguel et al, ).…”

“…(Ancylostomatidae) is delivered from the mother to pups through the milk, stays in the small intestine of the pups for 2 months, and then the parasite either dies along with its host or is cleared from the gut through an immune‐mediated mechanism (Seguel & Gottdenker, ; Seguel, Montalva et al, ; Seguel et al, ). In many otariid populations, the prevalence of hookworm infection is close to 100% (Seguel & Gottdenker, ), and total mortality can be up to 20% of all pups born in a season (Lyons et al, ; Seguel, Montalva et al, ). This high mortality is associated with the aggressive feeding behavior of the adult parasites, which cause deep wounds in the host intestine to feed on blood (Seguel et al, ; Seguel, Muñoz et al, ).…”

Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load

“…Furthermore, juveniles in our study population with low growth rates in the first 6 months of life have a lower probability of survival to adulthood than those with high growth rates (Hofer & East, ). High Ancylostoma infection loads are energetically costly because of substantial blood loss and damage to the intestinal wall (Urquhart et al, ), and have been reported to retard juvenile growth, and cause anemia and malnutrition in other mammals (Sakti et al, ; Seguel & Gottdenker, ; Stoltzfus et al, ). This suggests that the energetic cost of high Ancylostoma infection loads in rapidly growing, milk‐dependent juvenile hyenas may compromise growth and thus curtail survival to adulthood.…”

“…Our study aims to investigate determinants of both Ancylostoma (nematode) and Cystoisospora (coccidian) infection loads in high‐ranking and low‐ranking juvenile spotted hyenas and to assess the resistance and tolerance of juveniles in these two social categories to parasite infection. We focus on Ancylostoma and Cystoisospora because both have direct life cycles that need no intermediary host, both cause damage to the epithelial lining of the small intestine, and are considered energetically costly parasites (East et al, ; Seguel & Gottdenker, ; Shrestha et al, ). We test predictions derived from six hypotheses: (a) the resource allocation hypothesis of life‐history theory expects high‐ranking juveniles to have lower infection loads than low‐ranking juveniles, because they should have more resources to allocate to immune processes.…”