Michael V. K. Sukhdeo

Leaf-swallowing by chimpanzees: A behavioral adaptation for the control of strongyle nematode infections

Swallowing whole leaves by chimpanzees and other African apes has been hypothesized to have an antiparasitic or medicinal function, but detailed studies demonstrating this were lacking. We correlate for the first time quantifiable measures of the health of chimpanzees with observations of leaf-swallowing in Mahale Mountains National Park, Tanzania. We obtained a total of 27 cases involving the use ofAspilia mossambicensis (63%),Lippia plicata (7%),Hibiscus sp. (15%),Trema orientalis (4%), andAneilema aequinoctiale (11%), 15 cases by direct observation of 12 individuals of the Mahale M group. At the time of use, we noted behavioral symptoms of illness in the 8 closely observed cases, and detected single or multiple parasitic infections (Strongyloides fulleborni, Trichuris trichiura, Oesophagostomum stephanostomum) in 10 of the 12 individuals. There is a significant relationship between the presence of whole leaves (range, 1–51) and worms of adultO. stephanostomum (range, 2–21) in the dung. HPLC analysis of leaf samples collected after use showed that thiarubrine A, a compound proposed to act as a potent nematocide in swallowingAspilia spp., was not present in leaves ofA. mossambicensis or the three other species analyzed. Alternative nematocidal or egg-laying inhibition activity was not evident. Worms ofO. stephanostomum were recovered live and motile from chimpanzee dung, trapped within the folded leaves and attached to leaf surfaces by trichomes, though some were moving freely within the fecal matter, suggesting that the physical properties of leaves may contribute to the expulsion of parasites. We review previous hypotheses concerning leaf-swallowing and propose an alternative hypothesis based on physical action.

The behavioural ecology of parasites.

Parasites have evolved numerous complex and fascinating ways of interacting with their hosts. The subject attracts the interest of numerous biologists from the perspective of ecology and behavioral biology, as well as from those concerned with more applied aspects of parasitology. However, until now there has been no recent book to synthesize this field. This book, written by leading authorities from the USA, Europe, Australia and New Zealand, provides the most comprehensive coverage of this important topic on the market.

Parasite Behaviour: Understanding Platyhelminth Responses

Publisher Summary This chapter discusses parasite behavior in understanding platyhelminth responses. Parasitic organisms are similar to free-living organisms in that they respond to changes in their environment. These responses can take the form of measurable behavioral changes, underlying which there obviously has to be mechanisms involving the biochemistry and physiology of the parasitic organism. This chapter focuses on the importance of behavioral analyses to elucidate the mechanisms of orientation. In the free-living stages of parasitic platyhelminths, the ability to orient to specific cues is crucial. The host-finding behavior of the free-living miracidia involves at least three sequential steps where, at a minimum, the parasites must be able to respond directionally to cues that characterize the host habitat and the specific host. The long-term goal is to explain the reciprocal inhibition between the behavior of the pharynx (used in feeding) and the behavior of the ventral sucker (used in attachment and locomotion). The study of platyhelminth neurobiology can only advance through an approach that integrates behavioral analyses with neurobiology.

Hymenolepis diminuta: behavioral effects of 5-hydroxytryptamine, acetylcholine, histamine and somatostatin.

Consistent in vitro behavioral patterns were found in the scolex and strobila of adult Hymenolepis diminuta. These patterns were measured with a force transducer and the behavior analyzed with a slow motion closed circuit T.V. Varying concentrations of serotonin (5-HT), acetylcholine (Ach), histamine and somatostatin, in the range of 10(-3) to 10(-9) M, were tested for their influence on the rhythmic patterns of behavior. High concentrations of 5-HT and of Ach decreased scolex motility. While 5-HT significantly increased motility in the anterior-, mid- and posterior regions of the strobila at 10(-3) M, Ach inhibited motility in all 3 regions of the strobila at the same concentrations. At high concentrations, somatostatin had a smaller stimulatory effect on worm motility in the anterior and mid-regions; histamine only significantly affected worm motility in the posterior region of the strobila. Depending on concentration, the action of 5-HT, Ach and histamine can be reversed, particularly in the anterior and posterior regions of the strobila. The in vivo assay for worm migrational responses suggests that the action of the neuromuscular stimulators and inhibitors on worm migration is indirect.

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.

THE FOOD RESOURCE OF ADULT HELIGMOSOMOIDES POLYGYRUS IN THE SMALL INTESTINE

The aim of this study was to identify the food resources of Heligmosomoides polygyrus, a gastrointestinal nematode of mice. Gastrointestinal nematodes obtain food from 1 of 3 compartments: host ingesta, blood, or intestinal tissue. A method was developed to label these compartments differentially in the living host using 2 fluorescent marker dyes and to record in situ feeding activity of the parasite. Fluoresbrite is a yellow-green fluorescent dye bound to small-diameter beads that are membrane impermeable. Thus, it is restricted to the bloodstream when introduced there, or it remains in the ingesta when fed to the host. Rhodamine B, a red fluorescent dye, is membrane permeable and stains tissue cytoplasm. These dyes were fed to or injected into the bloodstream of the host. Following treatment, the worms were removed, and the contents of the worm intestines were examined by fluorescent microscopy. Worm intestinal contents only fluoresced with rhodamine B dye. These results suggest that H. polygyrus adults feed on tissue in the living host and not on host ingesta or blood.

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.

THE BEHAVIOR OF JUVENILE FASCIOLA HEPATICA

The behavioral repertoire of the infective stage of Fasciola hepatica was qualitatively characterized. During activation, a primary activity was the emptying of the ceca by peristaltic-like contractions. Emergence behavior comprised coordinated patterns of body movement and sucker activity specifically directed at disruption of the ventral plug. The stimulus specificity of the emergence response for glycine-conjugated cholic acid and the log dose-effect relationship of this response with glycocholic acid suggested a receptor-mediated sensory recognition. Extracts from the duodenum (departure organ) and the liver (arrival site) significantly affected the rate of locomotion and the orientation of the migratory stage. The evidence for orientation in the migrating stages is unequivocal, but the mechanisms by which they orient are unclear.

Critical resources that influence habitat selection decisions by gastrointestinal helminth parasites

Habitat selection may be the basis of some of the most exciting questions in behavioural ecology today, but parasites are being excluded from this debate. Parasites are not aberrant; they form a large proportion of the diversity of life on earth, and one estimate suggests that parasitism is more common than all other feeding strategies combined. We still do not understand the adaptive value of habitat selection behaviours in these organisms, even though the literature is full of examples of parasites migrating and navigating through hosts to their specific habitats. Parasites must make the same decisions that every animal has to make regarding food acquisition, shelter and reproduction. However, we cannot even make reasonable guesses on the habitat selection strategies and critical resources that influence their decision-making. The purpose of this review is to provide examples of experiments and methods of incorporating critical resources into the ecological analyses of habitat selection by gastrointestinal parasites. Information on parasite resources is simply not available for most parasites, and these ideas might stimulate and guide future research. In addition, parasites are ideal models to test theoretical assumptions of habitat selection. Experimental manipulations of parasites are ideal models to test theoretical assumptions of habitat selection. Experimental manipulations of parasite populations are simple, and habitats of endoparasites can be precisely altered by surgical methods. Few tests of habitat selection theory have been attempted in free-living environments because of the difficulty of assessing the correlations between environmental variations and organismal success in real-world situations, but this is not a problem with parasites because their habitats are replicated exactly in each host.

Host Centrality in Food Web Networks Determines Parasite Diversity

Background Parasites significantly alter topological metrics describing food web structure, yet few studies have explored the relationship between food web topology and parasite diversity. Methods/Principal Findings This study uses quantitative metrics describing network structure to investigate the relationship between the topology of the host food web and parasite diversity. Food webs were constructed for four restored brackish marshes that vary in species diversity, time post restoration and levels of parasitism. Our results show that the topology of the food web in each brackish marsh is highly nested, with clusters of generalists forming a distinct modular structure. The most consistent predictors of parasite diversity within a host were: trophic generality, and eigenvector centrality. These metrics indicate that parasites preferentially colonise host species that are highly connected, and within modules of tightly interacting species in the food web network. Conclusions/Significance These results suggest that highly connected free-living species within the food web may represent stable trophic relationships that allow for the persistence of complex parasite life cycles. Our data demonstrate that the structure of host food webs can have a significant effect on the establishment of parasites, and on the potential for evolution of complex parasite life cycles.