Alexander D. Hernandez

Monkeys in the Middle: Parasite Transmission through the Social Network of a Wild Primate

In wildlife populations, group-living is thought to increase the probability of parasite transmission because contact rates increase at high host densities. Physical contact, such as social grooming, is an important component of group structure, but it can also increase the risk of exposure to infection for individuals because it provides a mechanism for transmission of potentially pathogenic organisms. Living in groups can also create variation in susceptibility to infection among individuals because circulating levels of immunosuppressive hormones like glucocorticoids often depend on an individual’s position within the group’s social structure. Yet, little is known about the relative roles of socially mediated exposure versus susceptibility in parasite transmission among free-living animal groups. To address this issue, we investigate the relationship between host dominance hierarchy and nematode parasite transmission among females in a wild group of Japanese macaques (Macaca fuscata yakui). We use social network analysis to describe each individual female’s position within the grooming network in relation to dominance rank and relative levels of infection. Our results suggest that the number of directly-transmitted parasite species infecting each female, and the relative amount of transmission stages that one of these species sheds in faeces, both increase with dominance rank. Female centrality within the network, which shows positive associations with dominance hierarchy, is also positively associated with infection by certain parasite species, suggesting that the measured rank-bias in transmission may reflect variation in exposure rather than susceptibility. This is supported by the lack of a clear relationship between rank and faecal cortisol, as an indicator of stress, in a subset of these females. Thus, socially mediated exposure appears to be important for direct transmission of nematode parasites, lending support to the idea that a classical fitness trade-off inherent to living in groups can exist.

Parasites alter the topology of a stream food web across seasons.

Relatively few published food webs have included parasites, and in this study we examined the animal community in a stream across eight contiguous seasons to test how inclusion of helminth parasites alters the topology or structure of the food web. Food webs constructed for each season and analyzed using common binary matrix measures show that species richness, linkage density, and the number of observed and possible links increased when parasites were included as individual species nodes. With parasite–parasite and predator–parasite links omitted, measures of community complexity, such as connectance (C), generally increased over multiple seasons. However, relative nestedness (n*) decreased when parasites were included, which may be a result of low resolution of basal resources inflating specialist-to-specialist links. Overall, adding parasites resulted in moderate changes in food web measures when compared to those of four other published food webs representing different ecosystems. In addition, including parasites in the food web revealed consistent pathways of energy flow, and the association of parasite life histories along these pathways suggest stable evolutionary groups of interacting species within the community.

Host Grooming and the Transmission Strategy of Heligmosomoides polygyrus

Grooming behavior may play a part in the transmission of the gastrointestinal nematode, Heligomosomoides polygyrus in the mouse host. After infective larvae are placed on individually housed mice, significantly higher numbers of adult worms were recovered from the small intestine of mice that were allowed to self-groom when compared to infection levels in mice that had been fitted with Elizabethan collars to prevent self-grooming. Larvae placed on a single mouse housed with 3 other untreated mice resulted in all mice in the group becoming infected, suggesting that allogrooming may also be important in parasite transmission. A significantly higher percentage of larvae nictate on rough surfaces such as damp peat moss substrate when compared to smooth surfaces such as 0.5% agarose. Mice exposed to larvae placed on peat moss substrate have significantly higher infection levels when compared to mice exposed to larvae on a 0.5% agarose substratum, suggesting that natural transmission of infective L3 larvae in mice may be dependent on a substratum type that allows nictation behavior. A significantly higher percentage of worms were attracted to mouse urine and mouse and rat epidermal lipids when compared to deionized water controls in an in vitro preference assay, suggesting an attraction to host-specific signals. These results support the hypothesis that transmission of this parasite is an active process involving movement of the infective larvae of H. polygyrus into the hosts active space where they are ingested during grooming behavior.

Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques

Parasites are characteristically aggregated within hosts, but identifying the mechanisms underlying such aggregation can be difficult in wildlife populations. We examined the influence of host age and sex over an annual cycle on the eggs per gram of feces (EPG) of nematode parasites infecting wild Japanese macaques (Macaca fuscata yakui) on Yakushima Island. Five species of nematode were recorded from 434 fecal samples collected from an age-structured group of 50 individually recognizable macaques. All parasites exhibited aggregated EPG distributions. The age–infection profiles of all three directly transmitted species (Oesophagostomum aculeatum, Strongyloides fuelleborni, and Trichuris trichiura) exhibited convex curves, but concavity better characterized the age–infection curves of the two trophically transmitted species (Streptopharagus pigmentatus and Gongylonema pulchrum). There was a male bias in EPG and prevalence of infection with directly transmitted species, except in the prevalence of O. aculeatum, and no sex bias in the other parasites. Infection with O. aculeatum showed a female bias in prevalence among young adults, and additional interactions with sex and seasonality show higher EPG values in males during the mating season (fall) but in females during the birth season (spring). These patterns suggest that an immunosuppressive role by reproductive hormones may be regulating direct, but not indirect, life-cycle parasites. Exposure at an early age may trigger an immune response that affects all nematodes, but trophically transmitted species appear to accumulate thereafter. Although it is difficult to discern clear mechanistic explanations for parasite distributions in wildlife populations, it is critical to begin examining these patterns in host species that are increasingly endangered by anthropogenic threats.

Composition and diversity patterns in metazoan parasite communities and anthropogenic disturbance in stream ecosystems

The composition and diversity of metazoan parasite communities in naturally depauperate ecosystems are rarely studied. This study describes the composition of helminth endoparasite communities infecting fish that are part of naturally acidic stream ecosystems in the coastal-plains region of the State of New Jersey (USA) known as the Pinelands, and compares the diversity of parasites between six streams that differ in anthropogenic disturbance. A total of 514 fish were examined representing 6 species native but restricted to the Pinelands region, 5 species native and widespread throughout the region and State, and 6 species introduced to the Pinelands and State. Fish (prevalence: 78%) were infected with 18 helminth endoparasite species. In most streams, prevalence of infection, mean abundance, and total number of individuals for the 5 most common parasites were higher in pirate perch, a native fish species. The diversity of helminth endoparasite communities measured as species richness and Shannon index was higher in degraded streams, and especially in native or introduced fish at these sites. Parasite diversity was positively correlated with anthropogenic disturbance, which was measured by water pH, water conductance, and the proportion of agricultural and developed land surrounding streams. Helminth community composition included parasites intimately tied to trophic interactions in food webs, and disturbance to these ecosystems results in changes to these communities. Understanding structure and function of animal communities from these naturally depauperate ecosystems is important before continued anthropogenic changes result in the extirpation or extinction of their unique fauna.

Climate changes influence free-living stages of soil-transmitted parasites of European rabbits

Climate warming has been suggested to augment the risk of infectious disease outbreaks by extending the seasonal window for parasite growth and by increasing the rate of transmission. Understanding how this occurs in parasite-host systems is important for appreciating long-term and seasonal changes in host exposure to infection and to reduce species extinction caused by diseases. We investigated how free-living stages of two soil-transmitted helminths of the European rabbit (Oryctolagus cuniculus) responded to experimental changes in temperature by performing laboratory experiments with environmental chambers and field manipulations using open-top-chambers. This study was motivated by our previous observations that air temperature has increased over the last 30 years in our field site and that during this period intensity of infection of Graphidium strigosum but not Trichostrongylus retortaeformis was positively associated with this temperature increase. Laboratory and field experiments showed that both parasites accelerated egg development and increased hatching rate and larval survival in response to accumulating thermal energy. Both parasites behaved similarly when exposed to diverse temperature regimes, decadal trends, and monthly fluctuations, however, T. retortaeformis was more successful than G. strigosum by showing higher rates of egg hatching and larval survival. Across the months, the first day of hatching occurred earlier in warmer conditions suggesting that climate warming can lengthen the period of parasite growth and host exposure to infective stages. Also, T. retortaeformis hatched earlier than G. strigosum. These findings showed that seasonal changes in intensity, frequency, and duration of daily temperature are important causes of variability in egg hatching and larva survival. Overall, this study emphasizes the important role of climate warming and seasonality on the dynamics of free-living stages in soil-transmitted helminths and their contribution to enhance host exposure to parasitic infections. Yet, the ability to infect might ultimately depend on how hosts interact with parasites.

Parasites and Dung Beetles as Ecosystem Engineers in a Forest Ecosystem

Dung beetles serve as the intermediate host for Streptopharagus pigmentatus, a nematode parasite that infects an old world primate, the Japanese Macaque (Macaca fuscata). This study compares the behaviors of infected and uninfected beetles in both transmission dynamics and the ecological role of the parasite. The results suggest that parasitism does not alter the beetle’s use of shelter or choice of substrate on Yakushima Island, Japan. However, infected beetles consume significantly less feces. Dung beetles remove the majority of fecal material in this forest ecosystem, eliminating breeding grounds for many insect pests and burying nutrients that are essential for plant health. Thus, the nematode parasite S. pigmentatus, by altering its host’s behavior, changes the availability of fecal resources to both plant and animal communities and should therefore be classified as an ecosystem engineer.

Seasonal patterns in the biology of Eubothrium salvelini infecting brook trout in a creek in lower Michigan

A total of 392 brook trout, Salvelinus fontinalis, and 211 slimy sculpin, Cottus cognatus, was examined for Eubothrium salvelini (Cestoda) from May 1995 through September 1996 from Sweetwater Creek, Michigan. No seasonal pattern in prevalence, intensity, and abundance of parasites in trout and sculpin was determined. However a seasonal pattern in the length and percent gravid E. salvelini in brook trout suggests that recruitment of this parasite occurs during late summer and early fall. During this time the procercoid in the copepod intermediate host is expected to be available in the environment for fish to recruit, but a total of 6,399 copepods was not infected. Gravid worms were not found in slimy sculpin, suggesting it is a paratenic or dead-end host. Detailed studies on the biology of parasites may be more indicative of seasonal transmission patterns than studies that only measure prevalence, abundance, and intensity.